Lysosomal iron liberation is responsible for the vulnerability of brain microglial cells to iron oxide nanoparticles: comparison with neurons and astrocytes

References

• Bouzier-Sore AK, Pellerin L. 2013. Unraveling the complex metabolic nature of astrocytes. Front Cell Neurosci 7:179. doi: 10.3389/fncel.2013.00179
   PubMed Web of Science ®Google Scholar
• Caballero-Díaz E, Pfeiffer C, Kastl L, Rivera-Gil P, Simonet B, Valcárcel M, et al. 2013. The toxicity of silver nanoparticles depends on their uptake by cells and thus on their surface chemistry. Part Part Syst Charact 30:1079–85
   Web of Science ®Google Scholar
• Contestabile A. 2002. Cerebellar granule cells as a model to study mechanisms of neuronal apoptosis or survival in vivo and in vitro. Cerebellum 1:41–55
   PubMedGoogle Scholar
• Correale J. 2014. The role of microglial activation in disease progression. Mult Scler 20:1288–95
   PubMed Web of Science ®Google Scholar
• De Bock M, Decrock E, Wang N, Bol M, Vinken M, Bultynck G, Leybaert L. 2014. The dual face of connexin-based astroglial Ca2+ communication: a key player in brain physiology and a prime target in pathology. Biochim Biophys Acta 1843:2211–32
   PubMed Web of Science ®Google Scholar
• Dringen R. 2005. Oxidative and antioxidative potential of brain microglial cells. Antioxid Redox Signal 7:1223–33
   PubMed Web of Science ®Google Scholar
• Dringen R, Brandmann M, Hohnholt MC, Blumrich EM. 2015. Glutathione-dependent detoxification processes in astrocytes. Neurochem Res. [Epub ahead of print]. doi: 10.1007/s11064-014-1481-1
   Web of Science ®Google Scholar
• Dringen R, Kussmaul L, Hamprecht B. 1998. Detoxification of exogenous hydrogen peroxide and organic hydroperoxides by cultured astroglial cells assessed by microtiter plate assay. Brain Res Protoc 2:223–8
   PubMedGoogle Scholar
• Dringen R, Pawlowski P, Hirrlinger J. 2005. Peroxide detoxification by brain cells. J Neurosci Res 79:157–65
   PubMed Web of Science ®Google Scholar
• Dringen R, Scheiber IF, Mercer JF. 2013. Copper metabolism of astrocytes. Front Aging Neurosci 5:9. doi: 10.3389/fnagi.2013.00009
   PubMed Web of Science ®Google Scholar
• Dwivedi S, Siddiqui MA, Farshori NN, Ahamed M, Musarrat J, Al-Khedhairy AA. 2014. Synthesis, characterization and toxicological evaluation of iron oxide nanoparticles in human lung alveolar epithelial cells. Colloids Surf B Biointerfaces 122:209–15
   PubMed Web of Science ®Google Scholar
• Eyo UB, Dailey ME. 2013. Microglia: key elements in neural development, plasticity, and pathology. J Neuroimmune Pharmacol 8:494–509
   PubMed Web of Science ®Google Scholar
• Fernandes AR, Chari DM. 2014. A multicellular, neuro-mimetic model to study nanoparticle uptake in cells of the central nervous system. Integr Biol (Camb) 6:855–61
   PubMed Web of Science ®Google Scholar
• Fernandez-Fernandez S, Almeida A, Bolanos JP. 2012. Antioxidant and bioenergetic coupling between neurons and astrocytes. Biochem J 443:3–11
   PubMed Web of Science ®Google Scholar
• Geppert M, Hohnholt M, Gaetjen L, Grunwald I, Baumer M, Dringen R. 2009. Accumulation of iron oxide nanoparticles by cultured brain astrocytes. J Biomed Nanotechnol 5:285–93
   PubMed Web of Science ®Google Scholar
• Geppert M, Hohnholt MC, Thiel K, Nurnberger S, Grunwald I, Rezwan K, Dringen R. 2011. Uptake of dimercaptosuccinate-coated magnetic iron oxide nanoparticles by cultured brain astrocytes. Nanotechnology 22:145101. doi: 10.1088/0957-4484/22/14/145101
   PubMed Web of Science ®Google Scholar
• Geppert M, Hohnholt MC, Nurnberger S, Dringen R. 2012. Ferritin up-regulation and transient ROS production in cultured brain astrocytes after loading with iron oxide nanoparticles. Acta Biomater 8:3832–9
   PubMed Web of Science ®Google Scholar
• Geppert M, Petters C, Thiel K, Dringen R. 2013. The presence of serum alters the properties of iron oxide nanoparticles and lowers their accumulation by cultured brain astrocytes. J Nanopart Res 15:1349. doi: 10.1007/s11051-012-1349-8
   Web of Science ®Google Scholar
• Hanini A, Schmitt A, Kacem K, Chau F, Ammar S, Gavard J. 2011. Evaluation of iron oxide nanoparticle biocompatibility. Int J Nanomedicine 6:787–94
   PubMed Web of Science ®Google Scholar
• Hirrlinger J, Gutterer JM, Kussmaul L, Hamprecht B, Dringen R. 2000. Microglial cells in culture express a prominent glutathione system for the defense against reactive oxygen species. Dev Neurosci 22:384–92
   PubMed Web of Science ®Google Scholar
• Hohnholt M, Geppert M, Dringen R. 2010. Effects of iron chelators, iron salts, and iron oxide nanoparticles on the proliferation and the iron content of oligodendroglial OLN-93 cells. Neurochem Res 35:1259–68
   PubMed Web of Science ®Google Scholar
• Hohnholt MC, Dringen R. 2013. Uptake and metabolism of iron and iron oxide nanoparticles in brain astrocytes. Biochem Soc Trans 41:1588–92
   PubMed Web of Science ®Google Scholar
• Hühn D, Kantner K, Geidel C, Brandholt C, De Cock I, Soenen SJH, et al. 2013. Polymer-coated nanoparticles interacting with proteins and cells: focusing on the sign of the net charge. ACS Nano 7:3253–63
   PubMed Web of Science ®Google Scholar
• Jenkins SI, Pickard MR, Furness DN, Yiu HH, Chari DM. 2013. Differences in magnetic particle uptake by CNS neuroglial subclasses: implications for neural tissue engineering. Nanomedicine (Lond) 8:951–68
   PubMed Web of Science ®Google Scholar
• Kettenmann H, Hanisch UK, Noda M, Verkhratsky A. 2011. Physiology of microglia. Physiol Rev 91:461–553
   PubMed Web of Science ®Google Scholar
• Kinnunen TJJ, Haukka M, Pesonen E, Pakkanen TA. 2002. Ruthenium complexes with 2,2′-, 2,4′- and 4,4′-bipyridine ligands: the role of bipyridine coordination modes and halide ligands. J Organomet Chem 655:31–8
   Web of Science ®Google Scholar
• Kurz T, Eaton JW, Brunk UT. 2010. Redox activity within the lysosomal compartment: implications for aging and apoptosis. Antioxid Redox Signal 13:511–23
   PubMed Web of Science ®Google Scholar
• Lawen A, Lane DJ. 2013. Mammalian iron homeostasis in health and disease: uptake, storage, transport, and molecular mechanisms of action. Antioxid Redox Signal 18:2473–507
   PubMed Web of Science ®Google Scholar
• Lee JH, Ju JE, Kim BI, Pak PJ, Choi EK, Lee HS, Chung N. 2014. Rod-shaped iron oxide nanoparticles are more toxic than sphere-shaped nanoparticles to murine macrophage cells. Environ Toxicol Chem 33:2759–66
   PubMed Web of Science ®Google Scholar
• Levy M, Lagarde F, Maraloiu VA, Blanchin MG, Gendron F, Wilhelm C, Gazeau F. 2010. Degradability of superparamagnetic nanoparticles in a model of intracellular environment: follow-up of magnetic, structural and chemical properties. Nanotechnology 21:395103. doi: 10.1088/0957-4484/21/39/395103
   PubMed Web of Science ®Google Scholar
• Li L, Jiang W, Luo K, Song H, Lan F, Wu Y, Gu Z. 2013. Superparamagnetic iron oxide nanoparticles as MRI contrast agents for non-invasive stem cell labeling and tracking. Theranostics 3:595–615
   PubMed Web of Science ®Google Scholar
• Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. 1951. Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–75
   PubMed Web of Science ®Google Scholar
• Luther EM, Petters C, Bulcke F, Kaltz A, Thiel K, Bickmeyer U, Dringen R. 2013. Endocytotic uptake of iron oxide nanoparticles by cultured brain microglial cells. Acta Biomater 9:8454–65
   PubMed Web of Science ®Google Scholar
• Ma YM, De Groot H, Liu ZD, Hider RC, Petrat F. 2006. Chelation and determination of labile iron in primary hepatocytes by pyridinone fluorescent probes. Biochem J 395:49–55
   PubMed Web of Science ®Google Scholar
• Mahmoudi M, Stroeve P, Milani AS, Arbab AS. 2011. Superparamagnetic iron oxide nanoparticles: synthesis, surface engineering, cytotoxicity and biomedical applications. New York:Nova Science Publishers
   Google Scholar
• Maier-Hauff K, Ulrich F, Nestler D, Niehoff H, Wust P, Thiesen B, et al. 2011. Efficacy and safety of intratumoral thermotherapy using magnetic iron-oxide nanoparticles combined with external beam radiotherapy on patients with recurrent glioblastoma multiforme. J Neurooncol 103:317–24
   PubMed Web of Science ®Google Scholar
• Malvindi MA, De Matteis V, Galeone A, Brunetti V, Anyfantis GC, Athanassiou A, et al. 2014. Toxicity assessment of silica coated iron oxide nanoparticles and biocompatibility improvement by surface engineering. PLoS One 9:e85835. doi: 10.1371/journal.pone.0085835
   PubMed Web of Science ®Google Scholar
• Nau R, Ribes S, Djukic M, Eiffert H. 2014. Strategies to increase the activity of microglia as efficient protectors of the brain against infections. Front Cell Neurosci 8:138. doi: 10.3389/fncel.2014.00138
   PubMed Web of Science ®Google Scholar
• Nayak D, Roth TL, McGavern DB. 2014. Microglia development and function. Annu Rev Immunol 32:367–402
   PubMed Web of Science ®Google Scholar
• Nel A, Xia T, Mädler L, Li N. 2006. Toxic potential of materials at the nanolevel. Science 311:622–7
   PubMed Web of Science ®Google Scholar
• Neubert J, Wagner S, Kiwit J, Bräuer AU, Glumm J. 2015. New findings about iron oxide nanoparticles and their different effects on murine primary brain cells. Int J Nanomedicine 10:2033–49
   PubMed Web of Science ®Google Scholar
• Neuwelt EA, Varallyay P, Bago AG, Muldoon LL, Nesbit G, Nixon R. 2004. Imaging of iron oxide nanoparticles by MR and light microscopy in patients with malignant brain tumours. Neuropathol Appl Neurobiol 30:456–71
   PubMed Web of Science ®Google Scholar
• Peters DG, Connor JR. 2014. Introduction to cells comprising the nervous system. Adv Neurobiol 9:33–45
   PubMedGoogle Scholar
• Petters C, Bulcke F, Thiel K, Bickmeyer U, Dringen R. 2014a. Uptake of fluorescent iron oxide nanoparticles by oligodendroglial OLN-93 cells. Neurochem Res 39:372–83
   PubMed Web of Science ®Google Scholar
• Petters C, Dringen R. 2014. Comparison of primary and secondary rat astrocyte cultures regarding glucose and glutathione metabolism and the accumulation of iron oxide nanoparticles. Neurochem Res 39:46–58
   PubMed Web of Science ®Google Scholar
• Petters C, Dringen R. 2015. Accumulation of iron oxide nanoparticles by cultured primary neurons. Neurochem Int 81:1–9
   PubMed Web of Science ®Google Scholar
• Petters C, Irrsack E, Koch M, Dringen R. 2014b. Uptake and metabolism of iron oxide nanoparticles in brain cells. Neurochem Res 9:1648–60
   Web of Science ®Google Scholar
• Pickard MR, Chari DM. 2010. Robust uptake of magnetic nanoparticles (MNPs) by central nervous system (CNS) microglia: implications for particle uptake in mixed neural cell populations. Int J Mol Sci 11:967–81
   PubMed Web of Science ®Google Scholar
• Pierre JL, Fontecave M. 1999. Iron and activated oxygen species in biology: the basic chemistry. Biometals 12:195–9
   PubMed Web of Science ®Google Scholar
• Pinkernelle J, Calatayud P, Goya GF, Fansa H, Keilhoff G. 2012. Magnetic nanoparticles in primary neural cell cultures are mainly taken up by microglia. BMC Neurosci 13:32. doi: 10.1186/1471-2202-13-32
   PubMed Web of Science ®Google Scholar
• Poole B, Ohkuma S. 1981. Effect of weak bases on the intralysosomal pH in mouse peritoneal macrophages. J Cell Biol 90:665–9
   PubMed Web of Science ®Google Scholar
• Rathore KI, Redensek A, David S. 2012. Iron homeostasis in astrocytes and microglia is differentially regulated by TNF-alpha and TGF-beta1. Glia 60:738–50
   PubMed Web of Science ®Google Scholar
• Rivet CJ, Yuan Y, Borca-Tasciuc DA, Gilbert RJ. 2012. Altering iron oxide nanoparticle surface properties induce cortical neuron cytotoxicity. Chem Res Toxicol 25:153–61
   PubMed Web of Science ®Google Scholar
• Safi M, Courtois J, Seigneuret M, Conjeaud H, Berret JF. 2011. The effects of aggregation and protein corona on the cellular internalization of iron oxide nanoparticles. Biomaterials 32:9353–63
   PubMed Web of Science ®Google Scholar
• Saura J, Tusell JM, Serratosa J. 2003. High-yield isolation of murine microglia by mild trypsinization. Glia 44:183–9
   PubMed Web of Science ®Google Scholar
• Scalettar BA. 2006. How neurosecretory vesicles release their cargo. Neuroscientist 12:164–76
   PubMed Web of Science ®Google Scholar
• Scheiber IF, Mercer JF, Dringen R. 2010. Copper accumulation by cultured astrocytes. Neurochem Int 56:451–60
   PubMed Web of Science ®Google Scholar
• Stobart JL, Anderson CM. 2013. Multifunctional role of astrocytes as gatekeepers of neuronal energy supply. Front Cell Neurosci 7:38. doi: 10.3389/fncel.2013.00038
   PubMed Web of Science ®Google Scholar
• Sun Z, Yathindranath V, Worden M, Thliveris JA, Chu S, Parkinson FE, Hegmann T, Miller DW. 2013. Characterization of cellular uptake and toxicity of aminosilane-coated iron oxide nanoparticles with different charges in central nervous system-relevant cell culture models. Int J Nanomedicine 8:961–70
   PubMed Web of Science ®Google Scholar
• Taschner CA, Wetzel SG, Tolnay M, Froehlich J, Merlo A, Radue EW. 2005. Characteristics of ultrasmall superparamagnetic iron oxides in patients with brain tumors. AJR Am J Roentgenol 185:1477–86
   PubMed Web of Science ®Google Scholar
• Teplova VV, Tonshin AA, Grigoriev PA, Saris NE, Salkinoja-Salonen MS. 2007. Bafilomycin A1 is a potassium ionophore that impairs mitochondrial functions. J Bioenerg Biomembr 39:321–9
   PubMed Web of Science ®Google Scholar
• Tulpule K, Hohnholt MC, Hirrlinger J, Dringen R. (2014). Primary cultures of astrocytes and neurons as model systems to study the metabolism and metabolite export from brain cells. In: Waagepetersen HS, Hirrlinger J, eds. Neuromethods: Brain Energy Metabolism. Vol. 90. Heidelberg: Springer, 45–72
   Google Scholar
• Urrutia P, Aguirre P, Esparza A, Tapia V, Mena NP, Arredondo M, et al. 2013. Inflammation alters the expression of DMT1, FPN1 and hepcidin, and it causes iron accumulation in central nervous system cells. J Neurochem 126:541–9
   PubMed Web of Science ®Google Scholar
• van Landeghem FKH, Maier-Hauff K, Jordan A, Hoffmann KT, Gneveckow U, Scholz R, et al. 2009. Post-mortem studies in glioblastoma patients treated with thermotherapy using magnetic nanoparticles. Biomaterials 30:52–7
   PubMed Web of Science ®Google Scholar
• Verkhratsky A, Nedergaard M, Hertz L. 2014. Why are astrocytes important? Neurochem Res 40:389–401
   PubMed Web of Science ®Google Scholar
• Voinov MA, Pagan JOS, Morrison E, Smirnova TI, Smirnov AI. 2011. Surface-mediated production of hydroxyl radicals as a mechanism of iron oxide nanoparticle biotoxicity. J Am Chem Soc 133:35–41
   PubMed Web of Science ®Google Scholar
• Wang Y, Wang B, Zhu MT, Li M, Wang HJ, Wang M, et al. 2011. Microglial activation, recruitment and phagocytosis as linked phenomena in ferric oxide nanoparticle exposure. Toxicol Lett 205:26–37
   PubMed Web of Science ®Google Scholar
• Yan F, Wang Y, He SZ, Ku ST, Gu W, Ye L. 2013. Transferrin-conjugated, fluorescein-loaded magnetic nanoparticles for targeted delivery across the blood-brain barrier. J Mater Sci Mater Med 24:2371–9
   PubMed Web of Science ®Google Scholar
• Yang H, Liu C, Yang D, Zhang H, Xi Z. 2009. Comparative study of cytotoxicity, oxidative stress and genotoxicity induced by four typical nanomaterials: the role of particle size, shape and composition. J Appl Toxicol 29:69–78
   PubMed Web of Science ®Google Scholar