Skip to main content

Advertisement

SpringerLink
Log in

Oral intake of zirconia nanoparticle alters neuronal development and behaviour of Drosophila melanogaster

  • Research Paper
  • Published:
Journal of Nanoparticle Research Aims and scope Submit manuscript

Abstract

Zirconia nanoparticles (ZrO2 NPs) have been extensively used in teeth and bone implants and thus get a chance to interact with the physiological system. The current study investigated the oral administration of various concentrations of ZrO2 NPs synthesized by the hydrothermal method (0.25 to 5.0 mg L−1) on Drosophila physiology and behaviour. The size of the currently studied nanoparticle varies from 10 to 12 nm. ZrO2 NPs accumulated within the gut in a concentration-dependent manner and generate reactive oxygen species (ROS) only at 2.5 and 5.0 mg L−1 concentrations. ROS was detected by nitroblue tetrazolium (NBT) assay and 2′,7′-dichlorofluorescein (H2DCF) staining. The ROS toxicity alters the larval gut structure as revealed by DAPI staining. The NP stress of larvae affects the Drosophila development by distressing pupa count and varying the phenotypic changes in sensory organs (eye, thorax bristle, wings). Besides phenotypic changes, flawed climbing behaviour against gravity was seen in ZrO2 NP-treated flies. All together, for the first time, we have reported that a ROS-mediated ZrO2 NP toxicity alters neuronal development and functioning using Drosophila as a model organism.

ᅟ

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

Similar content being viewed by others

References

  • Aboushelib MN, Matinlinna JP, Salameh Z, Ounsi H (2008) Innovations in bonding to zirconia-based materials: part I. Dent Mater 24:1268–1272

    Article  Google Scholar 

  • Albanese A, Tang PS, Chan WC (2012) The effect of nanoparticle size, shape, and surface chemistry on biological systems. Annu Rev Biomed Eng 14:1–16

    Article  Google Scholar 

  • Al-Fahdawi MQ, Rasedee A, Al-Qubaisi MS, Alhassan FH, Rosli R, El Zowalaty ME, Naadja SE, Webster TJ, Taufiq-Yap YH (2015) Cytotoxicity and physicochemical characterization of iron–manganese-doped sulfated zirconia nanoparticles. Int J Nanomedicine 10:5739–5750

    Google Scholar 

  • Arefian Z, Pishbin F, Negahdary M, Ajdary M (2015) Potential toxic effects of zirconia oxide nanoparticles on liver and kidney factors. Biomed Res 26:89–97

    Google Scholar 

  • Armstrong N, Ramamoorthy M, Lyon D, Jones K, Duttaroy A (2013) Mechanism of silver nanoparticles action on insect pigmentation reveals intervention of copper homeostasis. PLoS One 8:e53186

    Article  Google Scholar 

  • Asadpour E, Sadeghnia HR, Ghorbani A, Sedaghat M, Boroushaki MT (2016) Oxidative stress-mediated cytotoxicity of zirconia nanoparticles on PC12 and N2a cells. J Nanopart Res 18:1–13

    Article  Google Scholar 

  • Barone MC, Bohmann D (2013) Assessing neurodegenerative phenotypes in Drosophila dopaminergic neurons by climbing assays and whole brain immunostaining. JoVE (J Vis Exp) e50339

  • Bokolia NP, Mishra M (2015) Hearing molecules, mechanism and transportation: modeled in Drosophila melanogaster. Dev Neurobiol 75:109–130

    Article  Google Scholar 

  • Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401–415

    Google Scholar 

  • Caicedo M, Jacobs JJ, Reddy A, Hallab NJ (2008) Analysis of metal ion-induced DNA damage, apoptosis, and necrosis in human (Jurkat) T-cells demonstrates Ni2+ and V3+ are more toxic than other metals: Al3+, Be2+, Co2+, Cr3+, Cu2+, Fe3+, Mo5+, Nb5+, Zr2+. J Biomed Mater Res A 86:905–913

    Article  Google Scholar 

  • Cant K, Knowles BA, Mooseker MS, Cooley L (1994) Drosophila singed, a fascin homolog, is required for actin bundle formation during oogenesis and bristle extension. J Cell Biol 125:369–380

    Article  Google Scholar 

  • Carinci F, Pezzetti F, Volinia S, Francioso F, Arcelli D, Farina E, Piattelli A (2004) Zirconium oxide: analysis of MG63 osteoblast-like cell response by means of a microarray technology. Biomaterials 25:215–228

    Article  Google Scholar 

  • Catelas I, Petit A, Zukor DJ, Marchand R, Yahia LH, Huk OL (1999) Induction of macrophage apoptosis by ceramic and polyethylene particles in vitro. Biomaterials 20:625–630

    Article  Google Scholar 

  • Clarke I, Manaka M, Green D, Williams P, Pezzotti G, Kim Y, Ries M, Sugano N, Sedel L, Delauney C (2003) Current status of zirconia used in total hip implants. J Bone Joint Surg 85:73–84

    Article  Google Scholar 

  • Claxton J (1969) Mosaic analysis of bristle displacement in Drosophila. Genetics 63:883–896

    Google Scholar 

  • Culí J, Martín-Blanco E, Modolell J (2001) The EGF receptor and N signalling pathways act antagonistically in Drosophila mesothorax bristle patterning. Development 128:299–308

    Google Scholar 

  • Depprich R, Zipprich H, Ommerborn M, Naujoks C, Wiesmann HP, Kiattavorncharoen S, Lauer HC, Meyer U, Kübler NR, Handschel J (2008) Osseointegration of zirconia implants compared with titanium: an in vivo study. Head Face Med 4:1–8

    Article  Google Scholar 

  • Di Virgilio A, Reigosa M, Arnal P, De Mele MFL (2010) Comparative study of the cytotoxic and genotoxic effects of titanium oxide and aluminium oxide nanoparticles in Chinese hamster ovary (CHO-K1) cells. J Hazard Mater 177:711–718

    Article  Google Scholar 

  • Fortini ME, Skupski MP, Boguski MS, Hariharan IK (2000) A survey of human disease gene counterparts in the Drosophila genome. J Cell Biol 150:23–30

    Article  Google Scholar 

  • Goodrich LV, Strutt D (2011) Principles of planar polarity in animal development. Development 138:1877–1892

    Article  Google Scholar 

  • Gupta SC, Siddique HR, Mathur N, Vishwakarma AL, Mishra RK, Saxena DK, Chowdhuri DK (2007) Induction of hsp70, alterations in oxidative stress markers and apoptosis against dichlorvos exposure in transgenic Drosophila melanogaster: modulation by reactive oxygen species. Biochim Biophys Acta 1770:1382–1394

    Article  Google Scholar 

  • Held LI (1991) Bristle patterning in Drosophila. BioEssays 13:633–640

    Article  Google Scholar 

  • Huang N, Yan Y, Xu Y, Jin Y, Lei J, Zou X, Ran D, Zhang H, Luan S, Gu H (2013) Alumina nanoparticles alter rhythmic activities of local interneurons in the antennal lobe of Drosophila. Nanotoxicology 7:212–220

    Article  Google Scholar 

  • Hussain S, Hess K, Gearhart J, Geiss K, Schlager J (2005) In vitro toxicity of nanoparticles in BRL 3A rat liver cells. Toxicol in Vitro 19:975–983

    Article  Google Scholar 

  • Karlsson HL, Cronholm P, Gustafsson J, Moller L (2008) Copper oxide nanoparticles are highly toxic: a comparison between metal oxide nanoparticles and carbon nanotubes. Chem Res Toxicol 21:1726–1732

    Article  Google Scholar 

  • Ko HC, Han JS, Bächle M, Jang JH, Shin SW, Kim DJ (2007) Initial osteoblast-like cell response to pure titanium and zirconia/alumina ceramics. Dent Mater 23:1349–1355

    Article  Google Scholar 

  • Kosmač T, Oblak C, Jevnikar P, Funduk N, Marion L (1999) The effect of surface grinding and sandblasting on flexural strength and reliability of Y-TZP zirconia ceramic. Dent Mater 1:426–433

    Article  Google Scholar 

  • Krebs RA, Feder ME (1997) Deleterious consequences of Hsp70 overexpression in Drosphila melanogaster larvae. Cell Stress Chaperones 2:60–71

    Article  Google Scholar 

  • Lacefield WR (1999) Materials characteristics of uncoated/ceramic-coated implant materials. Adv Dent Res 13:21–26

    Article  Google Scholar 

  • Lehane M (1997) Peritrophic matrix structure and function. Annu Rev Entomol 42:525–550

    Article  Google Scholar 

  • Lewinski N, Colvin V, Drezek R (2008) Cytotoxicity of nanoparticles. Small 4:26–49

    Article  Google Scholar 

  • Li Y, Fetchko M, Lai ZC, Baker NE (2003) Scabrous and Gp150 are endosomal proteins that regulate Notch activity. Development 130:2819–2827

    Article  Google Scholar 

  • Liang J, Deng Z, Jiang X, Li F, Li Y (2002) Photoluminescence of tetragonal ZrO2 nanoparticles synthesized by microwave irradiation. Inorg Chem 41:3602–3604

    Article  Google Scholar 

  • Lima EMCX, Koo H, Vacca Smith AM, Rosalen PL, Del Bel Cury AA (2008) Adsorption of salivary and serum proteins, and bacterial adherence on titanium and zirconia ceramic surfaces. Clin Oral Implants Res 19:780–785

    Article  Google Scholar 

  • Long TC, Saleh N, Tilton RD, Lowry GV, Veronesi B (2006) Titanium dioxide (P25) produces reactive oxygen species in immortalized brain microglia (BV2): implications for nanoparticle neurotoxicity. Environ Sci Technol 40:4346–4352

    Article  Google Scholar 

  • Lynch I, Dawson KA (2008) Protein-nanoparticle interactions. Nano Today 3:40–47

    Article  Google Scholar 

  • Manicone PF, Iommetti PR, Raffaelli L (2007) An overview of zirconia ceramics: basic properties and clinical applications. J Dent 35:819–826

    Article  Google Scholar 

  • Martinez V, Javadi C, Ngo E, Ngo L, Lagow R, Zhang B (2007) Age-related changes in climbing behavior and neural circuit physiology in Drosophila. Deve Neurobiol 67:778–791

    Article  Google Scholar 

  • Nagy LN, Mihály J, Polyák A, Debreczeni B, Császár B, Szigyártó IC, Wacha A, Czégény Z, Jakab E, Klébert S (2015) Inherently fluorescent and porous zirconia colloids: preparation, characterization and drug adsorption studies. J Mater Chem 3:7529–7537

    Article  Google Scholar 

  • Nagy LN, Polyák A, Mihály J, Szécsényi Á, Szigyártó IC, Czégény Z, Jakab E, Németh P, Magda B, Szabó PT (2016) Silica@zirconia@poly (malic acid) nanoparticle: a promising nanocarrier for theranostic applications. J Mater Chem B 4:4420–4429

    Article  Google Scholar 

  • Nichols CD, Becnel J, Pandey UB (2012) Methods to assay Drosophila behavior. JoVE (J Vis Exp) e3795

  • Ohlstein B, Spradling A (2006) The adult Drosophila posterior midgut is maintained by pluripotent stem cells. Nature 439:470–474

    Article  Google Scholar 

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

  • Piconi C, Maccauro G (1999) Zirconia as a ceramic biomaterial. Biomaterials 20:1–25

    Article  Google Scholar 

  • Posgai R, Cipolla-McCulloch CB, Murphy KR, Hussain SM, Rowe JJ, Nielsen MG (2011) Differential toxicity of silver and titanium dioxide nanoparticles on Drosophila Melanogaster development, reproductive effort, and viability: size, coatings and antioxidants matter. Chemosphere 85:34–42

    Article  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  Google Scholar 

  • 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. Altern Med Stud 2:2–6

    Article  Google Scholar 

  • Sollazzo V, Palmieri A, Pezzetti F, Bignozzi CA, Argazzi R, Massari L, Brunelli G, Carinci F (2008) Genetic effect of zirconium oxide coating on osteoblast-like cells. J Biomed Mater Res 84:550–558

    Article  Google Scholar 

  • Song W, Onishi M, Jan LY, Jan YN (2007) Peripheral multidendritic sensory neurons are necessary for rhythmic locomotion behavior in Drosophila larvae. Proc Natl Acad Sci 104:5199–5204

    Article  Google Scholar 

  • Sotoudeh A, Jahanshahi A, Takhtfooladi MA, Bazazan A, Ganjali A, Harati MP (2013) Study on nano-structured hydroxyapatite/zirconia stabilized yttria on healing of articular cartilage defect in rabbit. Acta Bras Cir 28:340–345

    Article  Google Scholar 

  • Sponchia G, Ambrosi E, Rizzolio F, Hadla M, Del Tedesco A, Spena CR, Toffoli G, Riello P, Benedetti A (2015) Biocompatible tailored zirconia mesoporous nanoparticles with high surface area for theranostic applications. J Mater Chem 3:7300–7306

    Article  Google Scholar 

  • Takashima S, Hartenstein V (2012) Genetic control of intestinal stem cell specification and development: a comparative view. Stem Cell Rev 8:597–608

    Article  Google Scholar 

  • Tang S, Huang X, Chen X, Zheng N (2010) Hollow mesoporous zirconia nanocapsules for drug delivery. Adv Funct Mater 20:2442–2447

    Article  Google Scholar 

  • Tsakonas A, Rand S, Matthew D, Lake JR (1999) Notch signaling: cell fate control and signal integration in development. Science 284:770–776

    Article  Google Scholar 

  • Wason MS, Colon J, Das S, Seal S, Turkson J, Zhao J, Baker CH (2013) Sensitization of pancreatic cancer cells to radiation by cerium oxide nanoparticle-induced ROS production. Nanomed Nanotech Biol Med 9:558–569

    Article  Google Scholar 

  • Wolff T, Ready DF (1991) Cell death in normal and rough eye mutants of Drosophila. Development 113:825–839

    Google Scholar 

  • Yang M, Hatton-Ellis E, Simpson P (2012) The kinase Sgg modulates temporal development of macrochaetes in Drosophila by phosphorylation of Scute and Pannier. Development 139:325–334

    Article  Google Scholar 

  • Zhang W, Yan Z, Li B, Jan LY, Jan YN (2014) Identification of motor neurons and a mechanosensitive sensory neuron in the defecation circuitry of Drosophila larvae. elife 3:e03293

    Google Scholar 

Download references

Acknowledgments

We are thankful to S. Aurosman Pappus for his help in larva video tracking. We are thankful to Prof. Santanu Paria laboratory for zeta potential analysis of the sample and technical staff of NIT Rourkela for handling SEM and TEM facility.

Author information

Authors and Affiliations

  1. Neural Developmental Biology Laboratory, Department of Life Science, National Institute of Technology, Rourkela, Odisha, 769008, India

    Monalisa Mishra, Debabrat Sabat & Swetapadma Sahu

  2. Department of Chemistry, National Institute of Technology, Rourkela, Odisha, 769008, India

    Basanti Ekka & Priyabrat Dash

  3. School of Biology, IISER Thiruvananthapuram, Trivandrum, Kerala, 695016, India

    Unnikannan P

Authors
  1. Monalisa Mishra
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Debabrat Sabat
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Basanti Ekka
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Swetapadma Sahu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Unnikannan P
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Priyabrat Dash
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Monalisa Mishra.

Ethics declarations

Funding

P. Unnikanan is thankful to DST-Inspire Fellowship for financial support.

Conflict of interest

The authors declare that they have no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mishra, M., Sabat, D., Ekka, B. et al. Oral intake of zirconia nanoparticle alters neuronal development and behaviour of Drosophila melanogaster . J Nanopart Res 19, 282 (2017). https://doi.org/10.1007/s11051-017-3971-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s11051-017-3971-y

Keywords

Search

Navigation