Top

Journal of Nanoparticle Research

Published in:

01-11-2012 | Research Paper

Involvement of reactive oxygen species and high-voltage-activated calcium currents in nanoparticle zinc oxide-induced cytotoxicity in vitro

Authors: Jingxia Zhao, Yang Yao, Shichang Liu, Tao Zhang, Guogang Ren, Zhuo Yang

Published in: Journal of Nanoparticle Research | Issue 11/2012

Activate our intelligent search to find suitable subject content or patents.

search-config

AI-assisted search

Off

Abstract

This study was to determine the possible neurotoxicity and mechanisms underlying the effects of nano-ZnO with sizes of 20–80 nm on central nervous system (CNS). The cytotoxicity of nano-ZnO was investigated in PC12 cells. The viability of cells was observed by a 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT) assay, and the generation of reactive oxygen species (ROS) for cells was evaluated by a fluorometry assay. The apoptosis of cells was detected and analyzed by flow cytometry. In addition, effects of nano-ZnO on the properties of high-voltage-activated (HVA) calcium currents were studied in acutely isolated rat hippocampal pyramidal neurons using the whole-cell patch clamp technique. The results of MTT assay showed that nano-ZnO (10⁻⁴ g/mL) caused a significant decrease in cell viability (P < 0.05). Nano-ZnO induced intracellular accumulation of ROS and the apoptosis of PC12 cells with the increasing concentration of nano-ZnO in flow cytometric assay (P < 0.05). Further results of electrophysiological recording indicated that 10⁻⁴ g/mL nano-ZnO first altered the current–voltage curve and the peak amplitudes of HVA calcium currents at 10 min of the recording, and the peak current amplitudes were increased significantly at the end of 30 min (P < 0.05). All these results suggested that the increase of intracellular ROS was one of potential mechanisms of cellular apoptosis induced by nano-ZnO. Nano-ZnO could cause the elevation of cytosolic calcium levels by enhancement of HVA calcium currents, which would increase the generation of intracellular ROS, and consequently promote the neuronal apoptosis.

previous article Quantifying the thermodynamic interactions of polyhedral boranes in solution to guide nanocomposite fabrication

next article Viscoelastic gels of guar and xanthan gum mixtures provide long-term stabilization of iron micro- and nanoparticles

Dont have a licence yet? Then find out more about our products and how to get one now:

Springer Professional "Wirtschaft+Technik"

Online-Abonnement

Mit Springer Professional "Wirtschaft+Technik" erhalten Sie Zugriff auf:

über 102.000 Bücher
über 537 Zeitschriften

aus folgenden Fachgebieten:

Automobil + Motoren
Bauwesen + Immobilien
Business IT + Informatik
Elektrotechnik + Elektronik
Energie + Nachhaltigkeit
Finance + Banking
Management + Führung
Marketing + Vertrieb
Maschinenbau + Werkstoffe
Versicherung + Risiko

Jetzt Wissensvorsprung sichern!

inform now

Springer Professional "Technik"

Online-Abonnement

Mit Springer Professional "Technik" erhalten Sie Zugriff auf:

über 67.000 Bücher
über 390 Zeitschriften

aus folgenden Fachgebieten:

Automobil + Motoren
Bauwesen + Immobilien
Business IT + Informatik
Elektrotechnik + Elektronik
Energie + Nachhaltigkeit
Maschinenbau + Werkstoffe

Jetzt Wissensvorsprung sichern!

inform now

Arundine M, Tymianski M (2003) Molecular mechanisms of calcium-dependent neurodegeneration in excitotoxicity. Cell Calcium 34:325–337. doi:10.1016/S0143-4160(03)00141-6 CrossRef

Beckman KB, Ames BN (1998) The free radical theory of aging matures. Physiol Rev 78:547–581

Bootman MD, Collins TJ, Peppiatt CM, Prothero LS, MacKenzie L, De Smet P, Travers M, Tovey SC, Seo JT, Berridge MJ, Ciccolini F, Lipp P (2001) Calcium signaling: an overview. Semin Cell Dev Biol 12:3–10. doi:10.1006/scdb.2000.0211 CrossRef

Bouron A, Boisseau S, De Waard M, Peris L (2006) Differential down-regulation of voltage-gated calcium channel currents by glutamate and BDNF in embryonic cortical neurons. Eur J Neurosci 24:699–708. doi:10.1111/j.1460-9568.2006.04946.x CrossRef

Brayner R, Ferrari-Iliou R, Brivois N, Djediat S, Benedetti MF, Fievet F (2006) Toxicological impact studies based on Escherichia coli bacteria in ultrafine ZnO nanoparticles colloidal medium. Nano Lett 6:866–870. doi:10.1021/nl052326h CrossRef

Brunner TJ, Wick P, Manser P, Spohn P, Grass RN, Limbach LK, Bruinink A, Stark WJ (2006) In vitro cytotoxicity of oxide nanoparticles: comparison to asbestos, silica, and the effect of particle solubility. Environ Sci Technol 40:4374–4381. doi:10.1021/es052069i CrossRef

Campbell LW, Hao SY, Thibault O, Blalock EM, Landfield PW (1996) Aging changes in voltage-gated calcium currents in hippocampal CA1 neurons. J Neurosci 16:6286–6295

Catterall WA (2000) Structure and regulation of voltage-gated Ca²⁺ channels. Annu Rev Cell Dev Biol 16:521–555CrossRef

Doering CJ, Zamponi GW (2003) Molecular pharmacology of high voltage-activated calcium channels. J Bioenerg Biomembr 35:491–505. doi:10.1023/B:JOBB.0000008022.50702.1a CrossRef

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 inhaled ultrafine manganese oxide particles to the central nervous system. Environ Health Perspect 114:1172–1178. doi:10.1289/ehp.9030 CrossRef

Elhamdani A, Bossu JL, Feltz A (1995) ADP exerts a protective effect against rundown of the Ca²⁺ current in bovine chromaffin cells. Pflug Arch Eur J Phy 430:401–409. doi:10.1007/BF00373916 CrossRef

Feissner RF, Skalska J, Gaum WE, Sheu SS (2009) Crosstalk signaling between mitochondrial Ca²⁺ and ROS. Front Biosci 14:1197–1218CrossRef

Franklin NM, Rogers NJ, Apte SC, Batley GE, Gadd GE, Casey PS (2007) Comparative toxicity of nanoparticulate ZnO, Bulk ZnO, and ZnCl₂ to a freshwater microalga (Pseudokirchneriella subcapitata): the importance of particle solubility. Environ Sci Technol 41:8484–8490. doi:10.1021/es071445r CrossRef

Furukawa K, Wang Y, Yao PJ, Fu W, Mattson MP, Itoyama Y, Onodera H, D’Souza I, Poorkaj PH, Bird TD, Schellenberg GD (2003) Alteration in calcium channel properties is responsible for the neurotoxic action of a familial frontotemporal dementia tau mutation. J Neurochem 87:427–436. doi:10.1046/j.1471-4159.2003.02020.x CrossRef

Ghule K, Ghule A, Chen BJ, Ling YC (2006) Preparation and characterization of ZnO nanoparticles coated paper and its antibacterial activity study. Green Chem 8:1034–1041. doi:10.1039/B605623G CrossRef

Green KN, Peers C (2002) Divergent pathways account for two distinct effects of amyloid β peptides on exocytosis and Ca²⁺ currents involvement of ROS and NF-κB. J Neurochem 81:1043–1051. doi:10.1046/j.1471-4159.2002.00907.x CrossRef

Green KN, Boyle JP, Peers C (2002) Hypoxia potentiates exocytosis and Ca²⁺ channels in PC12 cells via increased amyloid beta peptide formation and reactive oxygen species generation. J Physiol 541:1013–1023. doi:10.1113/jphysiol.2002.017582 CrossRef

Han D, Tian Y, Zhang T, Ren G, Yang Z (2011) Nano-zinc oxide damages spatial cognition capability via over-enhanced long-term potentiation in hippocampus of Wistar rats. Int J Nanomed 6:1453–1461. doi:10.2147/IJN.S18507

Heinlaan M, Ivask A, Blinova I, Dubourguier HC, Kahru A (2008) Toxicity of nanosized and bulk ZnO, CuO and TiO₂ to bacteria Vibrio fischeri and crustaceans Daphnia magna and Thamnocephalus platyurus. Chemosphere 71:1308–1316. doi:10.1016/j.chemosphere.2007.11.047 CrossRef

Jen J (1999) Calcium channelopathies in the central nervous system. Curr Opin Neurobiol 9:274–280. doi:10.1016/S0959-4388(99)80040-3 CrossRef

Jeng HA, Swanson J (2006) Toxicity of metal oxide nanoparticles in mammalian cells. J Environ Sci Health A 41:2699–2711. doi:10.1080/10934520600966177

Jiang W, Mashayekhi H, Xing B (2009) Bacterial toxicity comparison between nano- and micro-scaled oxide particles. Environ Pollut 157:1619–1625. doi:10.1016/j.envpol.2008.12.025 CrossRef

Kourie JI (1998) Interaction of reactive oxygen species with ion transport mechanisms. Am J Physiol 275:C1–C24

Lin WS, Xu Y, Huang CC, Ma Y, Shannon KB, Chen DR, Huang YW (2009) Toxicity of nano- and micro-sized ZnO particles in human lung epithelial cells. J Nanopart Res 11:25–39. doi:10.1007/s11051-008-9419-7 CrossRef

Lockman PR, Koziara JM, Mumper RJ, Allen DD (2004) Nanoparticle surface charges alter blood–brain barrier integrity and permeability. J Drug Target 12:635–641. doi:10.1080/10611860400015936 CrossRef

Long TC, Tajuba J, Sama P, Saleh N, Swartz C, Parker J, Hester S, Lowry GV, Veronesi B (2007) Nanosize titanium dioxide stimulates reactive oxygen species in brain microglia and damages neurons in vitro. Environ Health Perspect 115:1631–1637. doi:10.1289/ehp.10216 CrossRef

Ma H, Bertsch PM, Glenn TC, Kabengi NJ, Williams PL (2009) Toxicity of manufactured zinc oxide nanoparticles in the nematode Caenorhabditis elegans. Environ Toxicol Chem 28:1324–1330. doi:10.1897/08-262.1 CrossRef

Mattson MP (1996) Calcium and free radicals: mediators of neurotrophic factor and excitatory transmitter-regulated developmental plasticity and cell death. Perspect Dev Neurobiol 3:79–91

Mattson MP (2007) Calcium and neurodegeneration. Aging Cell 6:337–350. doi:10.1111/j.1474-9726.2007.00275.x CrossRef

Nel A, Xia T, Mädler L, Li N (2006) Toxic potential of materials at the nanolevel. Science 311:622–627. doi:10.1126/science.1114397 CrossRef

Oberdorster 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. doi:10.1080/08958370490439597 CrossRef

Ohkuma S, Katsura M, Higo A, Shirotani K, Hara A, Tarumi C, Ohgi T (2001) Peroxynitrite affects Ca²⁺ influx through voltage-dependent calcium channels. J Neurochem 76:341–350. doi:10.1046/j.1471-4159.2001.00045.x CrossRef

Peers C, Scragg JL, Boyle JP, Fearon IM, Taylor SC, Green KN, Webster NJ, Ramsden M, Pearson HA (2005) A central role for ROS in the functional remodelling of L-type Ca²⁺ channels by hypoxia. Philos Trans R Soc Lond B Biol Sci 360:2247–2254. doi:10.1098/rstb.2005.1761 CrossRef

Reddy KM, Feris K, Bell J, Wingett DG, Hanley C, Punnoose A (2007) Selective toxicity of zinc oxide nanoparticles to prokaryotic and eukaryotic systems. Appl Phys Lett 90:2139021–2139023. doi:10.1063/1.2742324

Sayes CM, Reed KL, Warheit DB (2007) Assessing toxicity of fine and nanoparticles: comparing in vitro measurements to in vivo pulmonary toxicity profiles. Toxicol Sci 97:163–180. doi:10.1093/toxsci/kfm018 CrossRef

Simon HU, Haj-Yehia A, Levi-Schaffer F (2000) Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis 5:415–418. doi:10.1023/A:1009616228304 CrossRef

Tam KH, Djurišić AB, Chan CMN, Xi YY, Tse CW, Leung YH, Chan WK, Leung FCC, Au DWT (2008) Antibacterial activity of ZnO nanorods prepared by a hydrothermal method. Thin Solid Films 516:6167–6174. doi:10.1016/j.tsf.2007.11.081 CrossRef

Turski L, Bressler K, Rettig KJ, Loschmann PA, Wachtel H (1991) Protection of substantia nigra from MPP+ neurotoxicity by N-methyl-d-aspartate antagonists. Nature 349:414–418CrossRef

Tymianski M, Wallace MC, Spigelman I, Uno M, Carlen PL, Tator CH, Charlton MP (1993) Cell-permeant Ca²⁺ chelators reduce early excitotoxic and ischemic neuronal injury in vitro and in vivo. Neuron 11:221–235. doi:10.1016/0896-6273(93)90180-Y CrossRef

Wagner JJ, Alger BE (1994) GTP modulates run-up of whole-cell Ca²⁺ channel current in a Ca²⁺-dependent manner. J Neurophysiol 71:814–816

Wang ZL (2008) Splendid one-dimensional nanostructures of zinc oxide: a new nanomaterial family for nanotechnology. ACS Nano 2:1987–1992. doi:10.1021/nn800631r CrossRef

Wang B, Feng WY, Wang M, Shi JW, Zhang F, Ouyang H, Zhao YL, Chai ZF, Huang YY, Xie YN, Wang HF, Wang J (2007) Transport of intranasally instilled fine Fe₂O₃ particles into the brain: micro-distribution, chemical states, and histopathological observation. Biol Trace Elem Res 118:233–243. doi:10.1007/s12011-007-0028-6 CrossRef

Wang B, Feng WY, Wang M, Wang TC, Gu YQ, Zhu MT, Ouyang H, Shi JW, Zhang F, Zhao YL, Chai ZF, Wang HF, Wang J (2008a) Acute toxicological impact of nano- and submicro-scaled zinc oxide powder on healthy adult mice. J Nanopart Res 10:263–276. doi:10.1007/s11051-007-9245-3 CrossRef

Wang JX, Chen CY, Liu Y, Jiao F, Li W, Lao F, Li YF, Li B, Ge CC, Zhou GQ, Gao Y, Zhao YL, Chai ZF (2008b) Potential neurological lesion after nasal instillation of TiO₂ nanoparticles in the anatase and rutile crystal phases. Toxicol Lett 183:72–80. doi:10.1016/j.toxlet.2008.10.001 CrossRef

Wang JX, Liu Y, Jiao F, Lao F, Li W, Gu YQ, Li YF, Ge CC, Zhou GQ, Li B, Zhao YL, Chai ZF, Chen CY (2008c) Time-dependent translocation and potential impairment on central nervous system by intranasally instilled TiO₂ nanoparticles. Toxicology 254:82–90. doi:10.1016/j.tox.2008.09.014 CrossRef

Wang B, Feng WY, Zhu MT, Wang Y, Wang M, Gu YQ, Ouyang H, Wang HJ, Li M, Zhao YL, Chai ZF, Wang HF (2009) Neurotoxicity of low-dose repeatedly intranasal instillation of nano- and submicron-sized ferric oxide particles in mice. J Nanopart Res 11:41–53. doi:10.1007/s11051-008-9452-6 CrossRef

Weiss JH, Hartley DM, Koh J, Choi DW (1990) The calcium channel blocker nifedipine attenuates slow excitatory amino acid neurotoxicity. Science 247:1474–1477CrossRef

Wiench K, Wohlleben W, Hisgen V, Radke K, Salinas E, Zok S, Landsiedel R (2009) Acute and chronic effects of nano- and non-nano-scale TiO₂ and ZnO particles on mobility and reproduction of the freshwater invertebrate Daphnia magna. Chemosphere 76:1356–1365. doi:10.1016/j.chemosphere.2009.06.025 CrossRef

Yamamoto O, Komatsu M, Sawai J, Nakagawa ZE (2004) Effect of lattice constant of zinc oxide on antibacterial characteristics. J Mater Sci Mater Med 15:847–851. doi:10.1023/B:JMSM.0000036271.35440.36 CrossRef

Yang Z, Liu ZW, Allaker R, Reip P, Oxford J, Ahmad Z, Ren G (2010) A review of nanoparticle functionality and toxicity on the central nervous system. J R Soc Interface 7:S411–S422. doi:10.1098/rsif.2010.0158.focus CrossRef

Zhang L, Jiang Y, Ding Y, Povey M, York D (2007) Investigation into the antibacterial behaviour of suspensions of ZnO nanoparticles (ZnO nanofluids). J Nanopart Res 9:479–489. doi:10.1007/s11051-006-9150-1 CrossRef

Zhao J, Xu L, Zhang T, Ren G, Yang Z (2009) Influences of nanoparticle zinc oxide on acutely isolated rat hippocampal CA3 pyramidal neurons. Neurotoxicology 30:220–230. doi:10.1016/j.neuro.2008.12.005 CrossRef

Zhu X, Zhu L, Duan Z, Qi R, Li Y, Lang Y (2008) Comparative toxicity of several metal oxide nanoparticle aqueous suspensions to Zebrafish (Danio rerio) early developmental stage. J Environ Sci Health A 43:278–284. doi:10.1080/10934520701792779

Title: Involvement of reactive oxygen species and high-voltage-activated calcium currents in nanoparticle zinc oxide-induced cytotoxicity in vitro
Authors: Jingxia Zhao
Yang Yao
Shichang Liu
Tao Zhang
Guogang Ren
Zhuo Yang
Publication date: 01-11-2012
Publisher: Springer Netherlands
Published in: Journal of Nanoparticle Research / Issue 11/2012
Print ISSN: 1388-0764
Electronic ISSN: 1572-896X
DOI: https://doi.org/10.1007/s11051-012-1238-1

Springer Professional

Abstract

Please log in to get access to your license.

Dont have a licence yet? Then find out more about our products and how to get one now:

Springer Professional "Wirtschaft+Technik"

Springer Professional "Technik"

Other articles of this Issue 11/2012

The direct writing and focusing of nanoparticles generated by an electrical discharge

Thermal evolution of Co on the coexisting Ag/Ge(111)- $$ \sqrt 3 \times \sqrt 3 $$ and Ag/Ge(111)-4 × 4 phases

New efficient five-input majority gate for quantum-dot cellular automata

Isolate, functionalize, and release: the ISOFURE platform for the functionalization of nanoparticles

Advanced functionalization of organoclay nanoparticles by silylation and their polystyrene nanocomposites obtained by miniemulsion polymerization

Nanoparticle manipulation within a microscale acoustofluidic droplet

Premium Partners