Abstract
Attractive due to an alleged high biocompatibility, silica nanoparticles have been widely used in the field of nanomedicine; however, their proven capacity to induce the synthesis and release of pro-inflammatory cytokines in several cellular models has raised concern about their safety. Glutamate, the main excitatory amino acid transmitter triggers a wide variety of signal transduction cascades that regulate protein synthesis at transcriptional and translational levels. A stimulus-dependent dynamic change in the protein repertoire in neurons and glia cells is the molecular framework of higher brain functions. Within the cerebellum, Bergmann glia cells are the most abundant non-neuronal cells and span the entire molecular layer of the cerebellar cortex, wrapping the synapses in this structure. Taking into consideration the functional role of Bergmann glia in terms of the recycling of glutamate, lactate supply to neurons, and prevention of neurotoxic insults, we decided to investigate the possibility that silica nanoparticles affect Bergmann glia and by these means alter the major excitatory neurotransmitter system in the brain. To this end, we exposed cultured chick cerebellar Bergmann glia cells to silica nanoparticles and measured [35S]-methionine incorporation into newly synthesized polypeptides. Our results demonstrate that exposure of the cultured cells to silica nanoparticles exerts a time- and dose-dependent modulation of protein synthesis. Furthermore, altered patterns of eukaryotic initiation factor 2 alpha and eukaryotic elongation factor 2 phosphorylation were present upon nanoparticle exposure. These results demonstrate that glia cells respond to the presence of this nanomaterial modifying their proteome, presumably in an effort to overcome any plausible neurotoxic effect.
Similar content being viewed by others
References
Aguirre A, López T, López-Bayghen E, Ortega A (2000) Glutamate regulates kainate-binding protein expression in cultured chick Bergmann glia through an activator protein-1 binding site. J Biol Chem 275:39246–39253. https://doi.org/10.1074/jbc.M002847200
Anderson JO, Thundiyil JG, Stolbach A (2012) Clearing the air: a review of the effects of particulate matter air pollution on human health. J Med Toxicol 8:166–175. https://doi.org/10.1007/s13181-011-0203-1
Araujo JA (2011) Particulate air pollution, systemic oxidative stress, inflammation, and atherosclerosis. Air Quality, Atmosphere & Health 4:79–93. https://doi.org/10.1007/s11869-010-0101-8
Barnes CA, Elsaesser A, Arkusz J, Smok A, Palus J, Lesniak A et al (2008) Reproducible comet assay of amorphous silica nanoparticles detects no genotoxicity. Nano Lett 8(9):3069–3074. https://doi.org/10.1021/nl801661w
Barrera I, Hernández-Kelly LC, Castelán F, Ortega A (2008) Glutamate-dependent elongation factor-2 phosphorylation in Bergmann glial cells. Neurochem Int 52:1167–1175
Blechinger J, Bauer AT, Torrano AA, Gorzelanny C, Bräuchle C, Schneider SW (2013) Uptake kinetics and nanotoxicity of silica nanoparticles are cell type dependent. Small 9(9):3970–3980. https://doi.org/10.1002/smll.201301004
Block ML, Calderón-Garcidueñas L (2009) Air pollution: mechanisms of neuroinflammation and CNS disease. Trends Neurosci 32:506–516. https://doi.org/10.1016/J.TINS.2009.05.009
Block ML, Elder A, Auten RL, Bilbo SD, Chen H, Chen JC, Cory-Slechta DA, Costa D, Diaz-Sanchez D, Dorman DC, Gold DR, Gray K, Jeng HA, Kaufman JD, Kleinman MT, Kirshner A, Lawler C, Miller DS, Nadadur SS, Ritz B, Semmens EO, Tonelli LH, Veronesi B, Wright RO, Wright RJ (2012) The outdoor air pollution and brain health workshop. NeuroToxicology 33:972–984. https://doi.org/10.1016/J.NEURO.2012.08.014
Brouwer D (2010) Exposure to manufactured nanoparticles in different workplaces. Toxicology. 269(2–3):120–127. https://doi.org/10.1016/j.tox.2009.11.017
Burnashev N, Khodorova A, Jonas P, Helm PJ, Wisden W, Monyer H, Seeburg PH, Sakmann B (1992) Calcium-permeable AMPA-kainate receptors in fusiform cerebellar glial cells. Science 256:1566–1569
Calderón-Garcidueñas L, Azzarelli B, Acuna H, Garcia R, Gambling TM, Osnaya N, Monroy S, DEL Tizapantzi MR, Carson JL, Villarreal-Calderon A, Rewcastle B (2002) Air pollution and brain damage. Toxicol Pathol 30:373–389. https://doi.org/10.1080/01926230252929954
Calderón-Garcidueñas L, Mora-Tiscareno A, Fordham LA, ValenciaSalazar G, Chung CJ, Rodriguez-Alcaraz A, Paredes R, Variakojis D, Villarreal-Calderón A, Flores-Camacho L, Antunez-Solis A, Henriquez-Roldan C, Hazucha MJ (2003) Respiratory damage in children exposed to urban pollution. Pediatr Pulmonol 36:148–161. https://doi.org/10.1002/ppul.10338
Calderón-Garcidueñas L, Reed W, Maronpot RR, Henriquez-Roldán C, Delgado-Chavez R, Calderón-Garcidueñas A, Dragustinovis I, Franco-Lira M, Aragón-Flores M, Solt AC, Altenburg M, Torres-Jardón R, Swenberg JA (2004) Brain inflammation and Alzheimer’s-like pathology in individuals exposed to severe air pollution. Toxicol Pathol 32:650–658. https://doi.org/10.1080/01926230490520232
Calderon-Garciduenas L, Reynoso-Robles R, Vargas-Martinez J, Gomez-Maqueo-Chew A, Perez-Guille B, Mukherjee PS, Torres-Jardon R, Perry G, Gonzalez-Maciel A (2016) Prefrontal white matter pathology in air pollution exposed Mexico City young urbanites and their potential impact on neurovascular unit dysfunction and the development of Alzheimer’s disease. Environ Res 146:404–417. https://doi.org/10.1016/j.envres.2015.12.031
Cammalleri M, Lutjens R, Berton F, King AR, Simpson C, Francesconi W, Sanna PP (2003) Time-restricted role for dendritic activation of the mTOR-p70S6K pathway in the induction of late-phase long-term potentiation in the CA1. Proc Natl Acad Sci 100:14368–14373. https://doi.org/10.1073/pnas.2336098100
Chen JC, Schwartz J (2009) Neurobehavioral effects of ambient air pollution on cognitive performance in US adults. Neurotoxicology 30:231–239. https://doi.org/10.1016/j.neuro.2008.12.011
Chen L, Yokel RA, Hennig B, Toborek M (2008) Manufactured aluminum oxide nanoparticles decrease expression of tight junction proteins in brain vasculature. J NeuroImmune Pharmacol 3:286–295. https://doi.org/10.1007/s11481-008-9131-5
Choi J, Zheng Q, Katz HE, Guilarte TR (2010) Silica-based nanoparticle uptake and cellular response by primary microglia. Environ Health Perspect 118(5):589–595. https://doi.org/10.1289/ehp.0901534
Christen V, Camenzind M, Fent K (2014) Silica nanoparticles induce endoplasmic reticulum stress response, oxidative stress and activate the mitogen-activated protein kinase (MAPK) signaling pathway. Toxicol Rep 1:1143–1151. https://doi.org/10.1016/j.toxrep.2014.10.023
Clogston JD, Patri AK (2011) Zeta potential measurement. In: McNeil S. (ed) Characterization of nanoparticles intended for drug delivery. Methods Molecular Biol (Methods and Protocols) 697:63–70. https://doi.org/10.1007/978-1-60327-198-1_6
Danbolt NC (2001) Glutamate uptake. Prog Neurobiol 65:1–105
Denizot F, Lang R (1986) Rapid colorimetric assay for cell growth and survival. Modifications to the tetrazolium dye procedure giving improved sensitivity and reliability. Journal of Immunological Methods 89:271–277. https://doi.org/10.1016/0022-1759(86)90368-6
Dorman DC, Brenneman KA, McElveen AM, Lynch SE, Roberts KC, Wong BA (2002) Olfactory transport: a direct route of delivery of inhaled manganese phosphate to the rat brain. J Toxicol Environ Health A 65:1493–1511. https://doi.org/10.1080/00984100290071630
Dosunmu R, Wu J, Basha MR, Zawia NH (2007) Environmental and dietary risk factors in Alzheimer’s disease. Expert Rev Neurother 7:887–900. https://doi.org/10.1586/14737175.7.7.887
Ducray AD, Stojiljkovic A, Möller A, Stoffel MH, Widmer HR, Frenz M, Mevissen M (2017) Uptake of silica nanoparticles in the brain and effects on neuronal differentiation using different in vitro models. Nanomedicine 13(3):1195–1204. https://doi.org/10.1016/j.nano.2016.11.001
Elder A, Gelein R, Silva V, Feikert T, Opanashuk L, Carter J, Potter R, Maynard A, Ito Y, Finkelstein J, Oberdörster G (2006) Translocation of inhale ultrafine manganese oxide particles to the central nervous system. Environ Health Perpect 114(8):1172–1178. https://doi.org/10.1289/ehp.9030
Environmental Protection Agency (1996) Air quality criteria for particulate matter. Office of Research and Development, Office of Health and Environmental Assessment, Research Triangle Park, N.C. EPA report no. EPA/600/P-95/001aF
Fagundes LS, Fleck Ada S, Zanchi AC, Saldiva PH, Rhoden CR (2015) Direct contact with particulate matter increases oxidative stress in different brain structures. Inhal Toxicol 27:462–467. https://doi.org/10.3109/08958378.2015.1060278
Farina F, Sancini G, Battaglia C, Tinaglia V, Mantecca P, Camatini M, Palestini P (2013) Milano summer particulate matter (PM10) triggers lung inflammation and extra pulmonary adverse events in mice. PLoS One 8:e56636. https://doi.org/10.1371/journal.pone.0056636.e56636
Flores-Méndez M, Ramírez D, Alamillo N, Hernández-Kelly LC, del Razo LM, Ortega A (2014) Fluoride exposure regulates the elongation phase of protein synthesis in cultured Bergmann glia cells. Toxicol Lett 229:126–133
Fu J, Gao J, Gong L, Ma Y, Xu H, Gu Z, Zhu J, Fan X (2018) Silica nanoparticle exposure during the neonatal period impairs hippocampal precursor proliferation and social behavior later in life. Int J Nanomedicine 13:3593–3608. https://doi.org/10.2147/IJN.S160828
Gary-Bobo M, Hocine O, Brevet D, Maynadier M, Raehm L, Richeter S, Charasson V, Loock B, Morère A, Maillard P, Garcia M, Durand JO (2012) Cancer therapy improvement with mesoporous silica nanoparticles combining targeting, drug delivery and PDT. Int J Pharm 423(2):509–515. https://doi.org/10.1016/j.ijpharm.2011.11.045
Geysen D, Vandecasteele C, Jaspers M, Wauters G (2004) Comparison of immobilisation of air pollution control residues with cement and with silica. J Hazard Mater 107(3):131–143. https://doi.org/10.1016/j.jhazmat.2003.12.001
Gonzalez-Mejia ME, Morales M, Hernandez-Kelly LCR et al (2006) Glutamate-dependent translational regulation in cultured Bergmann glia cells: involvement of p70S6K. Neuroscience 141:1389–1398
Guerra R, Vera-Aguilar E, Uribe-Ramirez M, Gookin G, Camacho J, Osornio-Vargas AR, Mugica-Alvarez V, Angulo-Olais R, Campbell A, Froines J, Kleinman TM, de Vizcaya-Ruiz A (2013) Exposure to inhaled particulate matter activates early markers of oxidative stress, inflammation and unfolded protein response in rat striatum. Toxicol Lett 222:146–154. https://doi.org/10.1016/j.toxlet.2013.07.012
Heneka MT, Rodríguez JJ, Verkhratsky A (2010) Neuroglia in neurodegeneration. Brain Res Rev 63(1–2):189–211. https://doi.org/10.1016/j.brainresrev.2009.11.004
Horie M, Fujita K (2011) Toxicity of metal oxides nanoparticles. Advances in Molecular Toxicology 5:145–178. https://doi.org/10.1016/B978-0-444-53864-2.00004-9
Hunter DD, Dey RD (1998) Identification and neuropeptide content of trigeminal neurons innervating the rat nasal epithelium. Neuroscience 83(2):591–599
Jo DH, Kim JH, Yu YS, Lee TG, Kim JH (2012) Antiangiogenic effect of silicate nanoparticles on retinal neovascularization induced by vascular endothelial growth factor. Nanomedicine 8(5):784–791. https://doi.org/10.1016/j.nano.2011.09.003
Kamikubo Y, Yamana T, Hashimoto Y, Sakurai T (2018) Induction of oxidative stress and cell death in neural cells by silica nanoparticles. ACS Chem Neurosci 10:304–312. https://doi.org/10.1021/acschemneuro.8b00248
Katsouyanni K, Pershagen G (1997) Ambient air pollution exposure and cancer. Cancer Causes Control 8:284–291. https://doi.org/10.1023/A:1018492818416
Katsouyanni K, Schwartz J, Spix C, Touloumi G, Zmirou D, Zanobetti A, Wojtyniak B, Vonk JM, Tobias A, Ponka A, Medina S, Bacharova L, Anderson HR (1996) Short term effects of air pollution on health: a European approach using epidemiologic time series data: the APHEA protocol. J Epidemiol Community Health 50:12–18. https://doi.org/10.1136/jech.50.Suppl_1.S12
Katz LC, Burkhalter A, Dreyer WJ (1984) Fluorescent latex microspheres as a retrograde neuronal marker for in vivo and in vitro studies of visual cortex. Nature 310:498–500
Kim IY, Joachim E, Choi H, Kim K (2015) Toxicity of silica nanoparticles depends on size, dose, and cell type. Nanomedicine 11(6):1407–1416. https://doi.org/10.1016/j.nano.2015.03.004
Kohane DS (2007) Microparticles and nanoparticles for drug delivery. Biotechnol Bioeng 96(2):203–209
Kozak M (2005) Regulation of translation via mRNA structure in prokaryotes and eukaryotes. Gene 361:13–37. https://doi.org/10.1016/j.gene.2005.06.037
Kurosinski P, Götz J (2002) Glial cells under physiologic and pathologic conditions. Arch Neurol 59(10):1524–1528. https://doi.org/10.1001/archneur.59.10.1524
Lai JCK, Ananthakrishnan G, Jandhyam S, Dukhande VV, Bhushan A, Gokhale M et al (2010) Treatment of human astrocytoma U87 cells with silicon dioxide nanoparticles lowers their survival and alters their expression on mitochondrial and cell signaling proteins. Int J Nanomedicine 5:715–723. https://doi.org/10.2147/IJN.S5238
Leung CC, Yu IT, Chen W (2012) Silicosis. Lancet 379(9830):2008–2018. https://doi.org/10.1016/S0140-6736(12)60235-9
Lin X, Zhao N, Yan P, Hu H, Xu F-J (2015) The shape and size effects of polycation functionalized silica nanoparticles on gene transfection. Acta Biomater 11:381–392. https://doi.org/10.1016/j.actbio.2014.09.004
Liu L, Wise DR, Diehl JA, Simon MC (2008) Hypoxic reactive oxygen species regulate the integrated stress response and cell survival. J Biol Chem 283:31153–31162. https://doi.org/10.1074/jbc.M805056200
López-Bayghen E, Ortega A (2004) Glutamate-dependent transcriptional regulation of GLAST: role of PKC. J Neurochem 91:200–209. https://doi.org/10.1111/j.1471-4159.2004.02706.x
López-Bayghen E, Rosas S, Castelán F, Ortega A (2007) Cerebellar Bergmann glia: an important model to study neuron-glia interactions. Neuron Glia Biol 3:155–167. https://doi.org/10.1017/S1740925X0700066X
Losacco C, Perillo A (2018) Particulate matter air pollution and respiratory impact on humans and animals. Environ Sci Pollut Res 25:33901–33910. https://doi.org/10.1007/s11356-018-3344-9
Lovisolo D, Dionisi M, Ruffinatti FA, Distasi C (2018) Nanoparticles and potential neurotoxicity: focus on molecular mechanisms. AIMS Molecular Science 5(1):1–13. https://doi.org/10.3934/molsci.2018.1.1
Marrache S, Dhar S (2012) Engineering of blended nanoparticle platform for delivery of mitochondria-acting therapeutics. Proc Natl Acad Sci U S A 109(40):16288–16293. https://doi.org/10.1073/pnas.1210096109
Martin KR (2007) The chemistry of silica and its potential health benefits. J Nutr Health Aging 11(2):94–98
Martínez-Lozada Z, Ortega A (2015) Glutamatergic transmission: a matter of three. Neural Plasticity 2015:1–11
Mendez-Flores OG, Hernández-Kelly LC, Suárez-Pozos E, Najimi M, Ortega A (2016) Coupling of glutamate and glucose uptake in cultured Bergmann glial cells. Neurochem Int 98:72–81
Mendoza A, Torres-Hernandez JA, Ault JG, Pedersen-Lane JH, Gao D, Lawrence DA (2014) Silica nanoparticles induce oxidative stress and inflammation of human peripheral blood mononuclear cells. Cell Stress Chaperones 19(6):777–790. https://doi.org/10.1007/s12192-014-0502-y
Merget R, Bauer T, Kupper HU, Philippou S, Bauer HD, Breitstadt R et al (2002) Health hazards due to the inhalation of amorphous silica. Arch Toxicol 75(11–12):625–634. https://doi.org/10.1007/s002040100266
Migliore L, Coppedè F (2009) Genetics, environmental factors and the emerging role of epigenetics in neurodegenerative diseases. Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis 667:82–97. https://doi.org/10.1016/j.mrfmmm.2008.10.011
Moon SL, Sonenberg N, Parker R (2018) Neuronal regulation of eIF2α function in health and neurological disorders. Trends Mol Med 24:575–589. https://doi.org/10.1016/j.molmed.2018.04.001
Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxic assay. J Immunol Methods 65:55–63
Napierska D, Thomassen LC, Lison D, Martens JA, Hoet PH (2010) The nanosilica hazard: another variable entity. Part Fibre Toxicol 7(1):39. https://doi.org/10.1186/1743-8977-7-39
Nemmar A, Yuvaraju P, Beegam S, Yasin J, Kazzam EE, Ali BH (2016) Oxidative stress, inflammation, and DNA damage in multiple organs of mice acutely exposed to amorphous silica nanoparticles. Int J Nanomedicine 11:919–928. https://doi.org/10.2147/IJN.S92278
Oberdörster G, Utell MJ (2002) Ultrafine particles in the urban air: to the respiratory tract—and beyond? Environ Health Perspect 110:A440–A441. https://doi.org/10.1289/ehp.110-a440
Oberdörster G, Sharp Z, Atudorei V, Elder A, Gelein R, Kreyling W, Cox C (2004) Translocation of inhaled ultrafine particles to the brain. Inhal Toxicol 16:437–445. https://doi.org/10.1080/08958370490439597
Orlando A, Cazzaniga E, Tringali M, Gullo F, Becchetti A, Minniti S, Taraballi F, Tasciotti E, Re F (2017) Mesoporous silica nanoparticles trigger mitophagy in endothelial cells and perturb neuronal network activity in a size- and time-dependent manner. Int J Nanomedicine 12:3547–3559. https://doi.org/10.2147/IJN.S127663
Ortega A, Eshhar N, Teichberg VI (1991) Properties of kainate receptor/channels on cultured Bergmann glia. Neuroscience 41:335–349. https://doi.org/10.1016/0306-4522(91)90331-H
Perea G, Sur M, Araque A (2014) Neuron-glia networks: integral gear of brain function. Front Cell Neurosci 8:378. https://doi.org/10.3389/fncel.2014.00378
Peters R, Kramer E, Oomen AG, Rivera ZE, Oegema G, Tromp PC, Fokkink R, Rietveld A, Marvi HJ, Weigel S et al (2012) Presence of nano-sized silica during in vitro digestion of foods containing silica as a food additive. ACS Nano 6:2441–2451
Pittenger C, Kandel E (1998) A genetic switch for long-term memory. C R Acad Sci III 321:91–96. https://doi.org/10.1016/S0764-4469(97)89807-1
Pope CA, Dockery DW (2006) Health effects of fine particulate air pollution: lines that connect. J Air Waste Manag Assoc 56:709–742. https://doi.org/10.1080/10473289.2006.10464485
Prokop A, Davidson JM (2008) Nanovehicular intracellular delivery systems. J Pharm Sci 97(9):3518–3590. https://doi.org/10.1002/jps.21270
Proud CG (2007) Signalling to translation: how signal transduction pathways control the protein synthetic machinery. Biochem J 403:217–234. https://doi.org/10.1042/BJ20070024
Ranft U, Schikowski T, Sugiri D, Krutmann J, Krämer U (2009) Long-term exposure to traffic-related particulate matter impairs cognitive function in the elderly. Environ Res 109:1004–1011. https://doi.org/10.1016/j.envres.2009.08.003
Rothen-Rutishauser B et al (2008) A newly developed in vitro model of the human epithelial airway barrier to study the toxic potential of nanoparticles. ALTEX 25:191–196. https://doi.org/10.14573/altex.2008.3.197
Roussel BD, Kruppa AJ, Miranda E, Crowther DC, Lomas DA, Marciniak SJ (2013) Endoplasmic reticulum dysfunction in neurological disease. Lancet Neurol 12(1):105–118. https://doi.org/10.1016/S1474-4422(12)70238-7
Ruiz M, Ortega A (1995) Characterization of an Na(+)-dependent glutamate/aspartate transporter from cultured Bergmann glia. Neuroreport 6(15):2041–2044
Ryazanov AG, Natapov PG, Shetakova EA, Severin FF, Spirin AS (1998) Phosphorylation of the elongation factor 2: the fifth Ca2+/calmodulin-dependent system of protein phosphorylation. Biochimie. 70(5):619–626. https://doi.org/10.1016/0300-9084(88)90245-3
Saffiotti U, Daniel L, Mao Y, Shi X, Williams A, Kaighn M (1994) Mechanisms of carcinogenesis by crystalline silica in relation to oxygen radicals. Environ Health Perspect 102:159–163. https://doi.org/10.1289/ehp.94102s10159
Schärtl W (2007) Light scattering from polymer solutions and nanoparticle dispersions. Springer, Berlin. https://doi.org/10.1007/978-3-540-71951-9_5
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675
Shank RP, Campbell GL (1984) Amino acid uptake, content, and metabolism by neuronal and glial enriched cellular fractions from mouse cerebellum. J Neurosci 4:58–69
Sharma S., Shukla P, Misra A., and Mishra PB (2014) Chapter 8—interfacial and colloidal properties of emulsifies systems: pharmaceutical and biological perspective. In book: Colloid and interface science in pharmaceutical research and development. 149–172. doi: https://doi.org/10.1016/B978-0-444-62614-1.0000-9
Sofroniew MV, Vinters HV (2010) Astrocytes: biology and pathology. Acta Neuropathol 119(1):7–35. https://doi.org/10.1007/s00401-009-0619-8
Somogyi P, Eshhar N, Teichberg VI, Roberts JDB (1990) Subcellular localization of a putative kainate receptor in Bergmann glial cells using a monoclonal antibody in the chick and fish cerebellar cortex. Neuroscience 35:9–30. https://doi.org/10.1016/0306-4522(90)90116-L
Sonenberg N, Hinnebusch AG (2009) Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 136:731–745. https://doi.org/10.1016/j.cell.2009.01.042
Wang J, Liu Y, Jiao F, Lao F, Li W, Gu Y, Li Y, Ge C, Zhou G, Li B, Zhao Y, Chai Z, Chen C (2008) Time-dependent translocation and potential impairment on central nervous system by instranasally instilled TiO(2) nanoparticles. Toxicology 254(1–2):82–90. https://doi.org/10.1016/j.tox.2008.09.014
Wang F, Jiao C, Liu J, Yuan H, Lan M, Gao F (2011) Oxidative mechanisms contribute to nanosize silican dioxide-induced developmental neurotoxicity in PC12 cells. Toxicol in Vitro 25(8):1548–1556. https://doi.org/10.1016/j.tiv.2011.05.019
Wang X, Rugufe da Mota S, Liu R, Moore CE, Xie J, Lanucara F, Agarwala U, Ruys SP, Vertommen D, Rider MH, Eyers CE, Proud CG (2014) Eukaryotic elongation factor 2 kinase activity is controlled by multiple inputs from oncogenic signaling. Mol Cell Biol 34:4088–4103. https://doi.org/10.1128/MCB.01035-14
Wang Y, Xiong L, Tang M (2017) Toxicity of inhaled particulate matter on the central nervous system: neuroinflammation, neuropsychological effects and neurodegenerative disease. J Appl Toxicol 37:644–667. https://doi.org/10.1002/jat.3451
Wang G, Li Y, Xu W, Yang Y, Tan X (2018) ROS mediated EGFR/MEK/ERK/HIF-1 α loop regulated glucose metabolism in pancreatic cancer. Biochem Biophys Res Commun 500:873–878. https://doi.org/10.1016/j.bbrc.2018.04.177
Wu J, Wang C, Sun J, Xue Y (2011) Neurotoxicity of silica nanoparticles: brain localization and dopaminergic neurons damage pathways. ACS Nano 5(6):4476–4489. https://doi.org/10.1021/nn103530b
Yan YL, Yang N, Xue-Fan GU (2013) Progress in research work on surface hydrophobic modification of silica nanoparticles and its effects of emulsification. China Surfactant Deterg Cosmet 43(3):224–231
Yang X, He C, Li J, Chen H, Ma Q, Sui X et al (2014) Uptake of silica nanoparticles: neurotoxicity and Alzheimer-like pathology in human SK-N-SH and mouse neuron2a neuroblastoma cells. Toxicol Lett 229(1):240–249. https://doi.org/10.1016/j.toxlet.2014.05.009
Ye Y, Liu J, Xu J, Sun L, Chen M, Lan M (2010) Nano-SiO2 induces apoptosis via activation of p53 and Bax mediated by oxidative stress in human hepatic cell line. Toxicol in Vitro 24(3):751–758. https://doi.org/10.1016/j.tiv.2010.01.001
You R, Ho Y-S, Hung CH-L, Liu Y, Huang C-X, Chan HN, Ho SL, Lui SY, Li HW, Chang RCC (2018) Silica nanoparticles induce neurodegeneration-like changes in behavior, neuropathology, and affect synapse through MAPK activation. Part Fibre Toxicol 15(1):28. https://doi.org/10.1186/s12989-018-0263-3
Zhao Y, Sun X, Zhang G, Trewyn BG, Slowing II, Lin VS (2011) Interaction of mesoporous silica nanoparticles with human red blood cells membranes: size and surface effects. ACS Nano 5(2):1366–1375. https://doi.org/10.1021/nn103077k
Acknowledgments
The technical assistance of Luis Cid and Blanca Ibarra is acknowledged.
Funding
This work was supported by grants from Consejo Nacional de Ciencia y Tecnología (Conacyt-México 255087) and Soluciones para un México Verde, S.A. to A.O. A.G.R.C. was supported by a Conacyt-México fellowship (no. 423462).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare that they have no conflicts of interest.
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
Rodríguez-Campuzano, A.G., Hernández-Kelly, L.C. & Ortega, A. Acute Exposure to SiO2 Nanoparticles Affects Protein Synthesis in Bergmann Glia Cells. Neurotox Res 37, 366–379 (2020). https://doi.org/10.1007/s12640-019-00084-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12640-019-00084-0