189
Views
3
CrossRef citations to date
0
Altmetric
Research Articles

Nano-CuO causes cell damage through activation of dose-dependent autophagy and mitochondrial lncCyt b-AS/ND5-AS/ND6-AS in SH-SY5Y cells

, , , , &
Pages 37-48 | Received 25 May 2021, Accepted 01 Aug 2021, Published online: 24 Aug 2021

References

  • Almansoori AA, Ju KW, Kim B, Kim SM, Lee S-M, Lee J-H. 2018. Hydroxyapatite coated magnesium alloy for peripheral nerve regeneration. Oral Biol Res. 42(3):105–113.
  • An L, Liu S, Yang Z, Zhang T. 2012. Cognitive impairment in rats induced by nano-CuO and its possible mechanisms. Toxicol Lett. 213(2):220–227.
  • Arakawa S, Honda S, Yamaguchi H, Shimizu S. 2017. Molecular mechanisms and physiological roles of Atg5/Atg7-independent alternative autophagy. Proc Jpn Acad Ser B Phys Biol Sci. 93(6):378–385.
  • Aruoja V, Dubourguier HC, Kasemets K, Kahru A. 2009. Toxicity of nanoparticles of CuO, ZnO and TiO2 to microalgae Pseudokirchneriella subcapitata. Sci Total Environ. 407(4):1461–1468.
  • Cheng Z, Du Z, Shang Y, Zhang Y, Zhang T. 2017. A preliminary study: PS1 increases U1 snRNA expression associated with AD. J Mol Neurosci. 62(3–4):269–275.
  • Cho WS, Duffin R, Poland CA, Howie SE, MacNee W, Bradley M, Megson IL, Donaldson K. 2010. Metal oxide nanoparticles induce unique inflammatory footprints in the lung: important implications for nanoparticle testing. Environ Health Perspect. 118(12):1699–1706.
  • Degterev A, Boyce M, Yuan J. 2003. A decade of caspases. Oncogene. 22(53):8543–8567.
  • Di Meco A, Curtis ME, Lauretti E, Praticò D. 2020. Autophagy dysfunction in Alzheimer’s disease: mechanistic insights and new therapeutic opportunities. Biol Psychiatry. 87(9):797–807.
  • Di Ruscio A, Ebralidze AK, Benoukraf T, Amabile G, Goff LA, Terragni J, Figueroa ME, De Figueiredo Pontes LL, Alberich-Jorda M, Zhang P, et al. 2013. DNMT1-interacting RNAs block gene-specific DNA methylation. Nature. 503(7476):371–376.
  • Dikic I, Elazar Z. 2018. Mechanism and medical implications of mammalian autophagy. Nat Rev Mol Cell Biol. 19(6):349–364.
  • Dykes IM, Emanueli C. 2017. Transcriptional and post-transcriptional gene regulation by long non-coding RNA. Genom Proteom Bioinformat. 15(3):177–186.
  • Fang K, Liu P, Dong S, Guo Y, Cui X, Zhu X, Li X, Jiang L, Liu T, Wu Y. 2016. Magnetofection based on superparamagnetic iron oxide nanoparticle-mediated low lncRNA HOTAIR expression decreases the proliferation and invasion of glioma stem cells. Int J Oncol. 49(2):509–518.
  • Farokhzad OC, Langer R. 2009. Impact of nanotechnology on drug delivery. ACS Nano. 3(1):16–20.
  • Gartler SM, Riggs AD. 1983. Mammalian X-chromosome inactivation. Annu Rev Genet. 17:155–190.
  • Godoy KF, Rodolpho JMA, Brassolatti P, Fragelli BDL, Castro CA, Assis M, Cancino Bernardi J, Correia RO, Albuquerque YR, Speglich C, et al. 2021. New multi-walled carbon nanotube of industrial interest induce cell death in murine fibroblast cells. Toxicol Mech Methods. 31(7):1–31.
  • Gomes T, Pereira CG, Cardoso C, Pinheiro JP, Cancio I, Bebianno MJ. 2012. Accumulation and toxicity of copper oxide nanoparticles in the digestive gland of Mytilus galloprovincialis. Aquat Toxicol. 118–119:72–79.
  • Grelet S, Link LA, Howley B, Obellianne C, Palanisamy V, Gangaraju VK, Diehl JA, Howe PH. 2017. A regulated PNUTS mRNA to lncRNA splice switch mediates EMT and tumour progression. Nat Cell Biol. 19(9):1105–1115.
  • Grote P, Wittler L, Hendrix D, Koch F, Währisch S, Beisaw A, Macura K, Bläss G, Kellis M, Werber M, et al. 2013. The tissue-specific lncRNA Fendrr is an essential regulator of heart and body wall development in the mouse. Dev Cell. 24(2):206–214.
  • He X, Deng H, Hwang HM. 2019. The current application of nanotechnology in food and agriculture. J Food Drug Anal. 27(1):1–21.
  • 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(7):1308–1316.
  • Hussey S, Travassos LH, Jones NL. 2009. Autophagy as an emerging dimension to adaptive and innate immunity. Semin Immunol. 21(4):233–241.
  • Jaggessar A, Shahali H, Mathew A, Yarlagadda P. 2017. Bio-mimicking nano and micro-structured surface fabrication for antibacterial properties in medical implants. J Nanobiotechnology. 15(1):64.
  • Jiang LC, Zhang WD. 2010. A highly sensitive nonenzymatic glucose sensor based on CuO nanoparticles-modified carbon nanotube electrode. Biosens Bioelectron. 25(6):1402–1407.
  • Joshi A, Naatz H, Faber K, Pokhrel S, Dringen R. 2020. Iron-doping of copper oxide nanoparticles lowers their toxic potential on C6 glioma cells. Neurochem Res. 45(4):809–824.
  • Ju C, Liu R, Zhang YW, Zhang Y, Zhou R, Sun J, Lv XB, Zhang Z. 2019. Mesenchymal stem cell-associated lncRNA in osteogenic differentiation. Biomed Pharmacother. 115:108912.
  • Kitchin KT, Richards JA, Robinette BL, Wallace KA, Coates NH, Castellon BT, Grulke EA, Kou J, Varma RS. 2020. Biochemical effects of silver nanomaterials in human hepatocellular carcinoma (HepG2) cells. J Nanosci Nanotechnol. 20(9):5833–5858.
  • Klionsky DJ, Abdelmohsen K, Abe A, Abedin MJ, Abeliovich H, Acevedo Arozena A, Adachi H, Adams CM, Adams PD, Adeli K, et al. 2016. Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition). Autophagy. 12(1):1–222.
  • Komatsu M, Wang QJ, Holstein GR, Friedrich VL, Iwata JI, Kominami E, Chait BT, Tanaka K, Yue Z. 2007. Essential role for autophagy protein Atg7 in the maintenance of axonal homeostasis and the prevention of axonal degeneration. Proc Natl Acad Sci USA. 104(36):14489–14494.
  • La Quaglia MP, Manchester KM. 1996. A comparative analysis of neuroblastic and substrate-adherent human neuroblastoma cell lines. J Pediatr Surg. 31(2):315–318.
  • Laha D, Pramanik A, Maity J, Mukherjee A, Pramanik P, Laskar A, Karmakar P. 2014. Interplay between autophagy and apoptosis mediated by copper oxide nanoparticles in human breast cancer cells MCF7. Biochim Biophys Acta. 1840(1):1–9.
  • Lamark T, Svenning S, Johansen T. 2017. Regulation of selective autophagy: the p62/SQSTM1 paradigm. Essays Biochem. 61(6):609–624.
  • Levine B, Kroemer G. 2019. Biological functions of autophagy genes: a disease perspective. Cell. 176(1–2):11–42.
  • Li P, Nijhawan D, Budihardjo I, Srinivasula SM, Ahmad M, Alnemri ES, Wang X. 1997. Cytochrome c and dATP-dependent formation of Apaf-1/caspase-9 complex initiates an apoptotic protease cascade. Cell. 91(4):479–489.
  • Li Z, Hao S, Yin H, Gao J, Yang Z. 2016. Autophagy ameliorates cognitive impairment through activation of PVT1 and apoptosis in diabetes mice. Behav Brain Res. 305:265–277.
  • Liang XH, Jackson S, Seaman M, Brown K, Kempkes B, Hibshoosh H, Levine B. 1999. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature. 402(6762):672–676.
  • Liu S, Xia T. 2020. Continued efforts on nanomaterial-environmental health and safety is critical to maintain sustainable growth of nanoindustry. Small. 16(21):e2000603.
  • Liu Z, Liu S, Ren G, Zhang T, Yang Z. 2011. Nano-CuO inhibited voltage-gated sodium current of hippocampal CA1 neurons via reactive oxygen species but independent from G-proteins pathway. J Appl Toxicol. 31(5):439–445.
  • Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 25(4):402–408.
  • Lopes VR, Loitto V, Audinot J-N, Bayat N, Gutleb AC, Cristobal S. 2016. Dose-dependent autophagic effect of titanium dioxide nanoparticles in human HaCaT cells at non-cytotoxic levels. J Nanobiotechnology. 14(1):22.
  • Ma X, Wu Y, Jin S, Tian Y, Zhang X, Zhao Y, Yu L, Liang XJ. 2011. Gold nanoparticles induce autophagosome accumulation through size-dependent nanoparticle uptake and lysosome impairment. ACS Nano. 5(11):8629–8639.
  • Martinou JC, Youle RJ. 2011. Mitochondria in apoptosis: Bcl-2 family members and mitochondrial dynamics. Dev Cell. 21(1):92–101.
  • Mishra AR, Zheng J, Tang X, Goering PL. 2016. Silver nanoparticle-induced autophagic-lysosomal disruption and NLRP3-inflammasome activation in HepG2 cells is size-dependent. Toxicol Sci. 150(2):473–487.
  • Mizushima N, Levine B. 2010. Autophagy in mammalian development and differentiation. Nat Cell Biol. 12(9):823–830.
  • Mizushima N, Yoshimori T. 2007. How to interpret LC3 immunoblotting. Autophagy. 3(6):542–545.
  • Mizushima N. 2007. Mizushima NAutophagy: process and function. Genes Dev. 21(22):2861–2873.
  • Modarresi F, Faghihi MA, Lopez-Toledano MA, Fatemi RP, Magistri M, Brothers SP, van der Brug MP, Wahlestedt C. 2012. Inhibition of natural antisense transcripts in vivo results in gene-specific transcriptional upregulation. Nat Biotechnol. 30(5):453–459.
  • Mohammadinejad R, Moosavi MA, Tavakol S, Vardar D, Hosseini A, Rahmati M, Dini L, Hussain S, Mandegary A, Klionsky DJ. 2019. Necrotic, apoptotic and autophagic cell fates triggered by nanoparticles. Autophagy. 15(1):4–33.
  • Murrow L, Debnath J. 2013. Autophagy as a stress-response and quality-control mechanism: implications for cell injury and human disease. Annu Rev Pathol. 8:105–137.
  • Oltvai ZN, Milliman CL, Korsmeyer SJ. 1993. Bcl-2 heterodimerizes in vivo with a conserved homolog, Bax, that accelerates programmed cell death. Cell. 74(4):609–619.
  • Pastori C, Peschansky VJ, Barbouth D, Mehta A, Silva JP, Wahlestedt C. 2014. Comprehensive analysis of the transcriptional landscape of the human FMR1 gene reveals two new long noncoding RNAs differentially expressed in Fragile X syndrome and Fragile X-associated tremor/ataxia syndrome. Hum Genet. 133(1):59–67.
  • Pattingre S, Tassa A, Qu X, Garuti R, Liang XH, Mizushima N, Packer M, Schneider MD, Levine B. 2005. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell. 122(6):927–939.
  • Pattison JS, Osinska H, Robbins J. 2011. Atg7 induces basal autophagy and rescues autophagic deficiency in CryABR120G cardiomyocytes. Circ Res. 109(2):151–160.
  • Petazzi P, Sandoval J, Szczesna K, Jorge OC, Roa L, Sayols S, Gomez A, Huertas D, Esteller M. 2013. Dysregulation of the long non-coding RNA transcriptome in a Rett syndrome mouse model. RNA Biol. 10(7):1197–1203.
  • Pickford F, Masliah E, Britschgi M, Lucin K, Narasimhan R, Jaeger PA, Small S, Spencer B, Rockenstein E, Levine B, et al. 2008. The autophagy-related protein beclin 1 shows reduced expression in early Alzheimer disease and regulates amyloid beta accumulation in mice. J Clin Invest. 118(6):2190–2199.
  • Rackham O, Shearwood AM, Mercer TR, Davies SM, Mattick JS, Filipovska A. 2011. Long noncoding RNAs are generated from the mitochondrial genome and regulated by nuclear-encoded proteins. RNA. 17(12):2085–2093.
  • Roy R, Singh SK, Chauhan LK, Das M, Tripathi A, Dwivedi PD. 2014. Zinc oxide nanoparticles induce apoptosis by enhancement of autophagy via PI3K/Akt/mTOR inhibition. Toxicol Lett. 227(1):29–40.
  • Ruoslahti E, Bhatia SN, Sailor MJ. 2010. Targeting of drugs and nanoparticles to tumors. J Cell Biol. 188(6):759–768.
  • Schaukowitch K, Kim TK. 2014. Emerging epigenetic mechanisms of long non-coding RNAs. Neuroscience. 264:25–38.
  • Siddiqui MA, Alhadlaq HA, Ahmad J, Al-Khedhairy AA, Musarrat J, Ahamed M. 2013. Copper oxide nanoparticles induced mitochondria mediated apoptosis in human hepatocarcinoma cells. PLoS One. 8(8):e69534.
  • Singh I, Sagare AP, Coma M, Perlmutter D, Gelein R, Bell RD, Deane RJ, Zhong E, Parisi M, Ciszewski J, et al. 2013. Low levels of copper disrupt brain amyloid-β homeostasis by altering its production and clearance. Proc Natl Acad Sci USA. 110(36):14771–14776.
  • Stern ST, Adiseshaiah PP, Crist RM. 2012. Autophagy and lysosomal dysfunction as emerging mechanisms of nanomaterial toxicity. Part Fibre Toxicol. 9:20.
  • Sun T, Yan Y, Zhao Y, Guo F, Jiang C. 2012. Copper oxide nanoparticles induce autophagic cell death in A549 cells. PLoS One. 7(8):e43442.
  • Vimbela GV, Ngo SM, Fraze C, Yang L, Stout DA. 2017. Antibacterial properties and toxicity from metallic nanomaterials. Int J Nanomedicine. 12:3941–3965.
  • Wang K, Liu CY, Zhou LY, Wang JX, Wang M, Zhao B, Zhao WK, Xu SJ, Fan LH, Zhang XJ, et al. 2015. APF lncRNA regulates autophagy and myocardial infarction by targeting miR-188-3p. Nat Commun. 6:6779.
  • Wang Q, Chen B, Ma F, Lin S, Cao M, Li Y, Gu N. 2017. Magnetic iron oxide nanoparticles accelerate osteogenic differentiation of mesenchymal stem cells via modulation of long noncoding RNA INZEB2. Nano Res. 10(2):626–642.
  • Wei P-F, Zhang L, Nethi SK, Barui AK, Lin J, Zhou W, Shen Y, Man N, Zhang Y-J, Xu J, et al. 2014. Accelerating the clearance of mutant huntingtin protein aggregates through autophagy induction by europium hydroxide nanorods. Biomaterials. 35(3):899–907.
  • Xicoy H, Wieringa B, Martens GJ. 2017. The SH-SY5Y cell line in Parkinson’s disease research: a systematic review. Mol Neurodegener. 12(1):10.
  • Xu H, Yuan R, Liu X, Li X, Qiao G, Li C, Gedanken A, Lin X. 2019. Zn-doped CuO nanocomposites inhibit tumor growth by NF-κB pathway cross-linked autophagy and apoptosis. Nanomedicine. 14(2):131–149.
  • Xu J, Li Z, Xu P, Xiao L, Yang Z. 2013. Nanosized copper oxide induces apoptosis through oxidative stress in podocytes. Arch Toxicol. 87(6):1067–1073.
  • Xu LJ, Zhao JX, Zhang T, Ren GG, Yang Z. 2009. In vitro study on influence of nano particles of CuO on CA1 pyramidal neurons of rat hippocampus potassium currents. Environ Toxicol. 24(3):211–217.
  • Yao RW, Wang Y, Chen LL. 2019. Cellular functions of long noncoding RNAs. Nat Cell Biol. 21(5):542–551.
  • Zhang X, Yin H, Li Z, Zhang T, Yang Z. 2016. Nano-TiO2 induces autophagy to protect against cell death through antioxidative mechanism in podocytes. Cell Biol Toxicol. 32(6):513–527.
  • Zhao J, Shi Q, Tian H, Li Y, Liu Y, Xu Z, Robert A, Liu Q, Meunier B. 2021. TDMQ20, a specific copper chelator, reduces memory impairments in Alzheimer’s disease mouse models. ACS Chem Neurosci. 12(1):140–149.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.