Skip to main content

Advertisement

SpringerLink
Log in

Oral administration of graphene oxide nano-sheets induces oxidative stress, genotoxicity, and behavioral teratogenicity in Drosophila melanogaster

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

The current study checks the effect of various concentrations of dietary graphene oxide (GO) nano-sheets on the development of Drosophila melanogaster. GO was synthesized and characterized by XRD, FTIR, FESEM, and TEM analytical techniques. Various concentrations of GO were mixed with the fly food and flies were transferred to the vial. Various behavioral and morphological as well as genetic defects were checked on the different developmental stages of the offspring. In the larval stage of development, the crawling speed and trailing path change significantly than the control. GO induces the generation of oxygen radicals within the larval hemolymph as evidenced by nitroblue tetrazolium assay. GO induces DNA damage within the gut cell, which was detected by Hoechst staining and within hemolymph by comet assay. Adult flies hatched after GO treatment show defective phototaxis and geotaxis behavior. Besides behavior, phenotypic defects were observed in the wing, eye, thorax bristles, and mouth parts. At 300 mg/L concentration, wing spots were observed. Altogether, the current study finds oral administration of GO which acts as a mutagen and causes various behavioral and developmental defects in the offspring. Here for the first time, we are reporting GO, which acts as a teratogen in Drosophila, besides its extensive medical applications.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Ahamed M, Posgai R, Gorey TJ, Nielsen M, Hussain SM, Rowe JJ (2010) Silver nanoparticles induced heat shock protein 70, oxidative stress and apoptosis in Drosophila melanogaster. Toxicol Appl Pharmacol 242:263–269

    Article  CAS  Google Scholar 

  • Augustyniak M, Gladysz M, Dziewięcka M (2016) The comet assay in insects—status, prospects and benefits for science. Mutat Res 767:67–76

    Article  CAS  Google Scholar 

  • Bae J-E, Bang S, Min S, Lee S-H, Kwon S-H, Lee Y, Lee Y-H, Chung J, Chae K-S (2016) Positive geotactic behaviors induced by geomagnetic field in Drosophila. Mol Brain 9:55

    Article  CAS  Google Scholar 

  • Barik BK, Mishra M (2018) Nanoparticles as a potential teratogen: a lesson learnt from fruit fly. Nanotoxicology:1–27

  • Bergin IL, Witzmann FA (2013) J Nanosci Nanotechnol 3:163–210

    CAS  Google Scholar 

  • Bhawal P, Ganguly S, Chaki T, Das N (2016) Synthesis and characterization of graphene oxide filled ethylene methyl acrylate hybrid nanocomposites. RSC Adv 6:20781–20790

    Article  CAS  Google Scholar 

  • Bianco A (2013) Graphene: safe or toxic? The two faces of the medal. Angew Chem 52:4986–4997

    Article  CAS  Google Scholar 

  • Bussy C, Al-Jamal KT, Boczkowski J, Lanone S, Prato M, Bianco A, Kostarelos K (2015) Microglia determine brain region-specific neurotoxic responses to chemically functionalized carbon nanotubes. ACS Nano 9:7815–7830

    Article  CAS  Google Scholar 

  • Campuzano S, Balcells L, Villares R, Carramolino L, García-Alonso L, Modolell J (1986) Excess function hairy-wing mutations caused by gypsy and copia insertions within structural genes of the achaete-scute locus of Drosophila. Cell 44:303–312

    Article  CAS  Google Scholar 

  • Carmona ER, Guecheva TN, Creus A, Marcos R (2011) Proposal of an in vivo comet assay using haemocytes of Drosophila melanogaster. Environ. Mol. Mutagen. 52:165–169

    Article  CAS  Google Scholar 

  • Carmona ER, Escobar B, Vales G, Marcos R (2015) Genotoxic testing of titanium dioxide anatase nanoparticles using the wing-spot test and the comet assay in Drosophila. Mutat Res Genet Toxicol Environ Mutagen 778:12–21

    Article  CAS  Google Scholar 

  • Chen Y, Hu X, Sun J, Zhou Q (2016) Specific nanotoxicity of graphene oxide during zebrafish embryogenesis. Nanotoxicology 10:42–52

    CAS  Google Scholar 

  • Chowdhury I, Duch MC, Mansukhani ND, Hersam MC, Bouchard D (2013) Colloidal properties and stability of graphene oxide nanomaterials in the aquatic environment. Environ Sci Technol 47:6288–6296

    Article  CAS  Google Scholar 

  • Chyb S, Gompel N (2013) Atlas of drosophila morphology: wild-type and classical mutants. Academic. Press

  • Cohen-Karni T, Qing Q, Li Q, Fang Y, Lieber CM (2010) Graphene and nanowire transistors for cellular interfaces and electrical recording. Nano Lett 10:1098–1102

    Article  CAS  Google Scholar 

  • Cui Y, Kim SN, Jones SE, Wissler LL, Naik RR, McAlpine MC (2010) Chemical functionalization of graphene enabled by phage displayed peptides. Nano Lett 10:4559–4565

    Article  CAS  Google Scholar 

  • Cui D, Mi L, Xu X, Lu J, Qian J, Liu S (2014) Nanocomposites of graphene and cytochrome P450 2D6 isozyme for electrochemical-driven tramadol metabolism. Langmuir 30:11833–11840

    Article  CAS  Google Scholar 

  • Czajka MC, Lee R (1990) A rapid cold-hardening response protecting against cold shock injury in Drosophila melanogaster. J Exp Biol 148:245–254

    CAS  Google Scholar 

  • Das P, McDonald JA, Petrof EO, Allen-Vercoe E, Walker VK (2014) Nanosilver-mediated change in human intestinal microbiota. J Nanomed Nanotechnol 5:1

    CAS  Google Scholar 

  • Dave SH, Gong C, Robertson AW, Warner JH, Grossman JC (2016) Chemistry and structure of graphene oxide via direct imaging. ACS Nano 10:7515–7522

    Article  CAS  Google Scholar 

  • De Celis JF (2002) Positioning and differentiation of veins in the Drosophila wing. Int J Dev Biol 42:335–343

    Google Scholar 

  • Demir E, Vales G, Kaya B, Creus A, Marcos R (2011) Genotoxic analysis of silver nanoparticles in Drosophila. Nanotoxicology 5:417–424

    Article  CAS  Google Scholar 

  • Demir E, Turna F, Vales G, Kaya B, Creus A, Marcos R (2013) In vivo genotoxicity assessment of titanium, zirconium and aluminium nanoparticles, and their microparticulated forms, in Drosophila. Chemosphere 93:2304–2310

    Article  CAS  Google Scholar 

  • Dhawan A, Bajpayee M, Parmar D (2009) Comet assay: a reliable tool for the assessment of DNA damage in different models. Cell Biol Toxicol 25:5–32

    Article  CAS  Google Scholar 

  • Frei H, Würgler FE (1988) Statistical methods to decide whether mutagenicity test data from Drosophila assays indicate a positive, negative, or inconclusive result. Mutation Research/Environmental Mutagenesis and Related Subjects, 203(4), pp.297-308.

  • Fröhlich EE, Fröhlich E (2016) Cytotoxicity of nanoparticles contained in food on intestinal cells and the gut microbiota. Int J Mol Sci 17:509

    Article  CAS  Google Scholar 

  • Gaivão I, Sierra LM (2014) Drosophila comet assay: insights, uses, and future perspectives. Front Genet 5:304

    Article  CAS  Google Scholar 

  • Gao W (2015) The chemistry of graphene oxide, Graphene Oxide. Springer, pp 61–95

  • Gao Y, Zou X, Zhao JX, Li Y, Su X (2013) Graphene oxide-based magnetic fluorescent hybrids for drug delivery and cellular imaging. Colloids Surf B Biointerfaces 112:128–133

    Article  CAS  Google Scholar 

  • Gao J, Zhang X, Yu M, Ren G, Yang Z (2015) Cognitive deficits induced by multi-walled carbon nanotubes via the autophagic pathway. Toxicology 337:21–29

    Article  CAS  Google Scholar 

  • Geim AK, Novoselov KS (2007) The rise of graphene. Nat Mater 6:183–191

    Article  CAS  Google Scholar 

  • Graf U, Würgler F, Katz A, Frei H, Juon H, Hall C, Kale P (1984) Somatic mutation and recombination test in Drosophila melanogaster. Environ Mutagen 6:153–188

    Article  CAS  Google Scholar 

  • Hällström I, Blanck A (1985) Genetic regulation of the cytochrome P-450 system in Drosophila melanogaster. I. Chromosomal determination of some cytochrome P-450-dependent reactions. Chem Biol Interact 56:157–171

    Article  Google Scholar 

  • He Q, Sudibya HG, Yin Z, Wu S, Li H, Boey F, Huang W, Chen P, Zhang H (2010) Centimeter-long and large-scale micropatterns of reduced graphene oxide films: fabrication and sensing applications. ACS Nano 4:3201–3208

    Article  CAS  Google Scholar 

  • Inada K, Kohsaka H, Takasu E, Matsunaga T, Nose A (2011) Optical dissection of neural circuits responsible for Drosophila larval locomotion with halorhodopsin. PloS one 6:e29019

    Article  CAS  Google Scholar 

  • Inagaki HK, Kamikouchi A, Ito K (2010) Protocol for quantifying sound-sensing ability of Drosophila melanogaster. Nat Protoc 5:26–30

    Article  CAS  Google Scholar 

  • Jambunathan N (2010) Determination and detection of reactive oxygen species (ROS), lipid peroxidation, and electrolyte leakage in plants, Plant Stress Tolerance. Springer, pp 291–297

  • Jana M, Saha S, Khanra P, Murmu NC, Srivastava SK, Kuila T, Lee JH (2014) Bio-reduction of graphene oxide using drained water from soaked mung beans (Phaseolus aureus L.) and its application as energy storage electrode material. Mater Sci Eng, B 186:33–40

    Article  CAS  Google Scholar 

  • Jatav VK, Agrawal D, Kumar S, Sharma S (2011) Lethal efficacy of acorus calamus in larval and adult stages of drosophila melanogaster. World 1:64–73

    CAS  Google Scholar 

  • Jha AN (2008) Ecotoxicological applications and significance of the comet assay. Mutagenesis 23:207–221

    Article  CAS  Google Scholar 

  • Johra FT, Lee J-W, Jung W-G (2014) Facile and safe graphene preparation on solution based platform. J Ind Eng Chem 20:2883–2887

    Article  CAS  Google Scholar 

  • Jones CF, Grainger DW (2009) In vitro assessments of nanomaterial toxicity. Adv Drug Deliv Rev 61:438–456

    Article  CAS  Google Scholar 

  • Kabiri Ameri S, Ho R, Jang H, Tao L, Wang Y, Wang L, Schnyer DM, Akinwande D, Lu N (2017) Graphene electronic tattoo sensors. ACS Nano 11:7634–7641

    Article  CAS  Google Scholar 

  • Kain JS, Stokes C, de Bivort BL (2012) Phototactic personality in fruit flies and its suppression by serotonin and white. PNAS USA 109:19834–19839

    Article  Google Scholar 

  • Kang K, Panzano VC, Chang EC, Ni L, Dainis AM, Jenkins AM, Regna K, Muskavitch MA, Garrity PA (2012) Modulation of TRPA1 thermal sensitivity enables sensory discrimination in Drosophila. Nature 481:76–80

    Article  CAS  Google Scholar 

  • Kellici S, Acord J, Ball J, Reehal HS, Morgan D, Saha B (2014) A single rapid route for the synthesis of reduced graphene oxide with antibacterial activities. RSC Adv. 4:14858–14861

    Article  CAS  Google Scholar 

  • Kolosnjaj-Tabi J, Hartman KB, Boudjemaa S, Ananta JS, Morgant G, Szwarc H, Wilson LJ, Moussa F (2010) In vivo behavior of large doses of ultrashort and full-length single-walled carbon nanotubes after oral and intraperitoneal administration to Swiss mice. ACS Nano 4:1481–1492

    Article  CAS  Google Scholar 

  • Krebs RA, Feder ME (1997) Deleterious consequences of Hsp70 overexpression in Drosphilla melanogaster larvae. Cell Stress Chaperones 2:60

    Article  CAS  Google Scholar 

  • Kuang L, Liu Y, Fu D, Zhao Y (2017) FeOOH-graphene oxide nanocomposites for fluoride removal from water: acetate mediated nano FeOOH growth and adsorption mechanism. J Colloid Interface Sci 490:259–269

    Article  CAS  Google Scholar 

  • Laird CD, McCarthy BJ (1968) Magnitude of interspecific nucleotide sequence variability in Drosophila. Genetics 60:303–322

    CAS  Google Scholar 

  • Liu Z, Robinson JT, Sun X, Dai H (2008) PEGylated nanographene oxide for delivery of water-insoluble cancer drugs. J Am Chem Soc 130:10876–10877

    Article  CAS  Google Scholar 

  • Liu J, Cui L, Losic D (2013) Graphene and graphene oxide as new nanocarriers for drug delivery applications. Acta Biomater 9:9243–9257

    Article  CAS  Google Scholar 

  • Liu L, Cui Z, Ma Q, Cui W, Zhang X (2016) One-step synthesis of magnetic iron–aluminum oxide/graphene oxide nanoparticles as a selective adsorbent for fluoride removal from aqueous solution. RSC Adv 6:10783–10791

    Article  CAS  Google Scholar 

  • Marcano DC, Kosynkin DV, Berlin JM, Sinitskii A, Sun Z, Slesarev A, Alemany LB, Lu W, Tour JM (2010) Improved synthesis of graphene oxide. ACS Nano 4:4806–4814

    Article  CAS  Google Scholar 

  • Marec F, Maťha V, Weiser J (1989) Analysis of the genotoxic activity of Bacillus thuringiensis β-exotoxin by means of the Drosophila wing spot test. J Invertebr Pathol 53:347–353

    Article  CAS  Google Scholar 

  • Mari E, Mardente S, Morgante E, Tafani M, Lococo E, Fico F, Valentini F, Zicari A (2016) Graphene oxide nanoribbons induce autophagic vacuoles in neuroblastoma cell lines. Int J Mol Sci 17:1995

    Article  CAS  Google Scholar 

  • Matsunaga T, Kohsaka H, Nose A (2017) Gap junction–mediated signaling from motor neurons regulates motor generation in the central circuits of larval Drosophila. J Neurosci 37:2045–2060

    Article  Google Scholar 

  • Mendes RG, Koch B, Bachmatiuk A, Ma X, Sanchez S, Damm C, Schmidt OG, Gemming T, Eckert J, Rümmeli MH (2015) A size dependent evaluation of the cytotoxicity and uptake of nanographene oxide. J Mater Chem B 3:2522–2529

    Article  CAS  Google Scholar 

  • Migliore L, Uboldi C, Di Bucchianico S, Coppedè F (2015) Nanomaterials and neurodegeneration. Environ Mol Mutagen 56:149–170

    Article  CAS  Google Scholar 

  • Mishra M, Barik BK (2018) Behavioral teratogenesis in Drosophila melanogaster, Teratogenicity Testing. Springer, pp 277–298

  • Mishra M, Sabat D, Ekka B, Sahu S, Unnikannan P, Dash P (2017) Oral intake of zirconia nanoparticle alters neuronal development and behaviour of Drosophila melanogaster. J Nanoparticle Res 19:282

    Article  CAS  Google Scholar 

  • Mushtaq G, A Khan J, Joseph E, A Kamal M (2015) Nanoparticles, neurotoxicity and neurodegenerative diseases. Curr Drug Metab 16:676–684

    Article  CAS  Google Scholar 

  • Olteanu D, Filip A, Socaci C, Biris AR, Filip X, Coros M, Rosu MC, Pogacean F, Alb C, Baldea I (2015) Cytotoxicity assessment of graphene-based nanomaterials on human dental follicle stem cells. Colloids Surf B: Biointerfaces 136:791–798

    Article  CAS  Google Scholar 

  • Ong C, Yung L-YL, Cai Y, Bay B-H, Baeg G-H (2015) Drosophila melanogaster as a model organism to study nanotoxicity. Nanotoxicology 9:396–403

    Article  CAS  Google Scholar 

  • Onoda A, Takeda K, Umezawa M (2018) Dysregulation of major functional genes in frontal cortex by maternal exposure to carbon black nanoparticle is not ameliorated by ascorbic acid pretreatment. Sci Total Environ 634:1126–1135

    Article  CAS  Google Scholar 

  • Pappus SA, Mishra M (2018) A Drosophila model to decipher the toxicity of nanoparticles taken through oral routes, cellular and molecular toxicology of nanoparticles. Springer, pp 311–322

  • Pappus SA, Ekka B, Sahu S, Sabat D, Dash P, Mishra M (2017) A toxicity assessment of hydroxyapatite nanoparticles on development and behaviour of Drosophila melanogaster. J Nanoparticle Res 19:136

    Article  CAS  Google Scholar 

  • Park S, Ruoff RS (2009) Chemical methods for the production of graphenes. Nat Nanotechnol 4:217–224

    Article  CAS  Google Scholar 

  • Petkau K, Parsons BD, Duggal A, Foley E (2014) A deregulated intestinal cell cycle program disrupts tissue homeostasis without affecting longevity in Drosophila. J Biol Chem 289:28719–28729

    Article  CAS  Google Scholar 

  • Philbrook NA, Walker VK, Afrooz AN, Saleh NB, Winn LM (2011) Investigating the effects of functionalized carbon nanotubes on reproduction and development in Drosophila melanogaster and CD-1 mice. Reprod Toxicol 32:442–448

    Article  CAS  Google Scholar 

  • Pompa PP, Vecchio G, Galeone A, Brunetti V, Sabella S, Maiorano G, Falqui A, Bertoni G, Cingolani R (2011) In vivo toxicity assessment of gold nanoparticles in Drosophila melanogaster. Nano Res 4:405–413

    Article  CAS  Google Scholar 

  • Pretti C, Oliva M, Di Pietro R, Monni G, Cevasco G, Chiellini F, Pomelli C, Chiappe C (2014) Ecotoxicity of pristine graphene to marine organisms. Ecotoxicol Environ Saf 101:138–145

    Article  CAS  Google Scholar 

  • Raj A, Shah P, Agrawal N (2017) Sedentary behavior and altered metabolic activity by AgNPs ingestion in Drosophila melanogaster. Sci Rep 7:15617

    Article  CAS  Google Scholar 

  • Rao CNR, Sood AK, Subrahmanyam KS, Govindaraj A (2009) Graphene: the new two-dimensional nanomaterial. Angew Chem Int Ed 48:7752–7777

    Article  CAS  Google Scholar 

  • Sabat D, Patnaik A, Ekka B, Dash P, Mishra M (2016) Investigation of titania nanoparticles on behaviour and mechanosensory organ of Drosophila melanogaster. Physiol Behav 167:76–85

    Article  CAS  Google Scholar 

  • Sanchez VC, Jachak A, Hurt RH, Kane AB (2011) Biological interactions of graphene-family nanomaterials: an interdisciplinary review. Chem Res Toxicol 25:15–34

    Article  CAS  Google Scholar 

  • Sawin-McCormack EP, Sokolowski MB, Campos AR (1995) Characterization and genetic analysis of Drosophila melanogaster photobehavior during larval development. J Neurogenet 10:119–135

    Article  CAS  Google Scholar 

  • Shao Y, Wang J, Wu H, Liu J, Aksay IA, Lin Y (2010) Graphene based electrochemical sensors and biosensors: a review. Electroanalysis 22:1027–1036

    Article  CAS  Google Scholar 

  • Shilpa S, Basavaraja BM, Majumder SB, Sharma A (2015) Electrospun hollow glassy carbon-reduced graphene oxide nanofibers with encapsulated ZnO nanoparticles: a free-standing anode for li-ion batteries, Meeting Abstracts. J Electrochem Soc:468–468

  • Siddique YH (2012) Protective role of curcumin against the toxic effects of cyclophosphamide in the third instar larvae of transgenic Drosophila melanogaster (hsp70-lacZ) Bg9. Alternative Medicine Studies 2:2

    Article  Google Scholar 

  • Siddique YH, Khan W, Khanam S, Jyoti S, Naz F, Singh BR, Naqvi AH (2014) Toxic potential of synthesized graphene zinc oxide nanocomposite in the third instar larvae of transgenic Drosophila melanogaster (hsp70-lacZ) Bg9. Biomed Res Int 2014:1–10

  • Sk MM, Yue CY (2014) Layer-by-layer (LBL) assembly of graphene with p-phenylenediamine (PPD) spacer for high performance supercapacitor applications. RSC Adv 4:19908–19915

    Article  CAS  Google Scholar 

  • Spence D, Peyman G (1976) A new technique for the vital staining of the corneal endothelium. Invest Ophthalmol Vis Sci 15:1000–1002

    CAS  Google Scholar 

  • Strober W (1997) Trypan blue exclusion test of cell viability. Curr Protoc Immunol. 21:A. 3B. 1–A. 3B. 2

    Google Scholar 

  • Szendi K, Varga C (2008) Lack of genotoxicity of carbon nanotubes in a pilot study. Anticancer Res 28:349–352

    CAS  Google Scholar 

  • Tang J, Huang Y, Gong Y, Lyu H, Wang Q, Ma J (2016) Preparation of a novel graphene oxide/Fe-Mn composite and its application for aqueous Hg (II) removal. J Hazard Mater 316:151–158

    Article  CAS  Google Scholar 

  • Vallabani N, Mittal S, Shukla RK, Pandey AK, Dhakate SR, Pasricha R, Dhawan A (2011) Toxicity of graphene in normal human lung cells (BEAS-2B). J Biomed Nanotechnol 7:106–107

    Article  CAS  Google Scholar 

  • Vang LL, Medvedev AV, Adler J (2012) Simple ways to measure behavioral responses of Drosophila to stimuli and use of these methods to characterize a novel mutant. PloS one 7:e37495

    Article  CAS  Google Scholar 

  • Wang Y, Li Z, Wang J, Li J, Lin Y (2011) Graphene and graphene oxide: biofunctionalization and applications in biotechnology. Trends Biotechnol 29:205–212

    Article  CAS  Google Scholar 

  • Wang J, Liang S, Ma L, Ding S, Yu X, Zhou L, Wang Q (2014) One-pot synthesis of CdS–reduced graphene oxide 3D composites with enhanced photocatalytic properties. Cryst Eng Comm 16:399–405

    Article  CAS  Google Scholar 

  • Wei Y, Zhou F, Zhang D, Chen Q, Xing D (2016) A graphene oxide based smart drug delivery system for tumor mitochondria-targeting photodynamic therapy. Nanoscale 8:3530–3538

    Article  CAS  Google Scholar 

  • Win-Shwe T-T, Fujimaki H (2011) Nanoparticles and neurotoxicity. Int. J. Mol. Sci. 12:6267–6280

    Article  CAS  Google Scholar 

  • Zhang Y, Ali SF, Dervishi E, Xu Y, Li Z, Casciano D, Biris AS (2010) Cytotoxicity effects of graphene and single-wall carbon nanotubes in neural phaeochromocytoma-derived PC12 cells. ACS Nano 4:3181–3186

    Article  CAS  Google Scholar 

  • Zhang Y, Wu C, Guo S, Zhang J (2013) Interactions of graphene and graphene oxide with proteins and peptides. Nanotechnol Rev 2:27–45

    Google Scholar 

  • Zhu Y, Murali S, Cai W, Li X, Suk JW, Potts JR, Ruoff RS (2010) Graphene and graphene oxide: synthesis, properties, and applications. Adv. Mater. 22:3906–3924

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Three anonymous reviewers are thankfully acknowledged for their valuable comments on the manuscript.

Funding

SP and SM received financial support from MHRD. SS received financial support from DST-Inspire. GH and MM received financial support from DBT (Grant No. BT/PR21857/NNT/28/1238/2017).

Author information

Authors and Affiliations

  1. Neural Developmental Biology Lab, Department of Life Science, NIT Rourkela, Rourkela, Odisha, 769008, India

    Subhashree Priyadarsini, Swetapadma Sahu, Sumit Mukherjee & Monalisa Mishra

  2. Department of Chemistry, NIT Rourkela, Rourkela, Odisha, 769008, India

    Shraban Kumar Sahoo & Garudadhwaj Hota

Authors
  1. Subhashree Priyadarsini
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shraban Kumar Sahoo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Swetapadma Sahu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sumit Mukherjee
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Garudadhwaj Hota
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Monalisa Mishra
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Monalisa Mishra.

Additional information

Responsible editor: Philippe Garrigues

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Priyadarsini, S., Sahoo, S.K., Sahu, S. et al. Oral administration of graphene oxide nano-sheets induces oxidative stress, genotoxicity, and behavioral teratogenicity in Drosophila melanogaster. Environ Sci Pollut Res 26, 19560–19574 (2019). https://doi.org/10.1007/s11356-019-05357-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-019-05357-x

Keywords

Search

Navigation