journal article·2017-08

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

Monalisa Mishra, Debabrat Sabat, Basanti Ekka, Swetapadma Sahu, Unnikannan P, Priyabrat Dash

Journal of Nanoparticle Research· Volume 19· Issue 8
Publisher page

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.
Source: openaire · Quality: candidate unverified · Source record ↗

Research context

OpenAlex topics: Nanoparticles: synthesis and applications · Marine Biology and Environmental Chemistry · Environmental Toxicology and Ecotoxicology

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

References (58)

Show source-provided references
1. Aboushelib MN, Matinlinna JP, Salameh Z, Ounsi H (2008) Innovations in bonding to zirconia-based materials: part I. Dent Mater 24:1268–127210.1016/j.dental.2008.02.010 ↗
2. Albanese A, Tang PS, Chan WC (2012) The effect of nanoparticle size, shape, and surface chemistry on biological systems. Annu Rev Biomed Eng 14:1–1610.1146/annurev-bioeng-071811-150124 ↗
3. 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
4. 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
5. 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:e5318610.1371/journal.pone.0053186 ↗
6. 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 18:1–1310.1007/s11051-015-3316-7 ↗
7. Barone MC, Bohmann D (2013) Assessing neurodegenerative phenotypes in Drosophila dopaminergic neurons by climbing assays and whole brain immunostaining. JoVE (J Vis Exp) e50339
8. Bokolia NP, Mishra M (2015) Hearing molecules, mechanism and transportation: modeled in Drosophila melanogaster. Dev Neurobiol 75:109–13010.1002/dneu.22221 ↗
9. Brand AH, Perrimon N (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401–41510.1242/dev.118.2.401 ↗
10. 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 86:905–91310.1002/jbm.a.31789 ↗
11. 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 125:369–38010.1083/jcb.125.2.369 ↗
12. 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 25:215–22810.1016/S0142-9612(03)00486-1 ↗
13. 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 20:625–63010.1016/S0142-9612(98)00214-2 ↗
14. 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 85:73–8410.2106/00004623-200300004-00009 ↗
15. Claxton J (1969) Mosaic analysis of bristle displacement in Drosophila. Genetics 63:883–89610.1093/genetics/63.4.883 ↗
16. Culí J, Martín-Blanco E, Modolell J (2001) The EGF receptor and N signalling pathways act antagonistically in Drosophila mesothorax bristle patterning. Development 128:299–30810.1242/dev.128.2.299 ↗
17. 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 4:1–810.1186/1746-160X-4-1 ↗
18. 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 177:711–71810.1016/j.jhazmat.2009.12.089 ↗
19. Fortini ME, Skupski MP, Boguski MS, Hariharan IK (2000) A survey of human disease gene counterparts in the Drosophila genome. J Cell Biol 150:23–3010.1083/jcb.150.2.F23 ↗
20. Goodrich LV, Strutt D (2011) Principles of planar polarity in animal development. Development 138:1877–189210.1242/dev.054080 ↗
21. 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 1770:1382–139410.1016/j.bbagen.2007.05.010 ↗
22. Held LI (1991) Bristle patterning in Drosophila. BioEssays 13:633–64010.1002/bies.950131203 ↗
23. 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 7:212–22010.3109/17435390.2011.648668 ↗
24. 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 19:975–98310.1016/j.tiv.2005.06.034 ↗
25. 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 21:1726–173210.1021/tx800064j ↗
26. 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 23:1349–135510.1016/j.dental.2006.11.023 ↗
27. 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 1:426–43310.1016/S0109-5641(99)00070-6 ↗
28. Krebs RA, Feder ME (1997) Deleterious consequences of Hsp70 overexpression in Drosphila melanogaster larvae. Cell Stress Chaperones 2:60–7110.1379/1466-1268(1997)002<0060:DCOHOI>2.3.CO;2 ↗
29. Lacefield WR (1999) Materials characteristics of uncoated/ceramic-coated implant materials. Adv Dent Res 13:21–2610.1177/08959374990130011001 ↗
30. Lehane M (1997) Peritrophic matrix structure and function. Annu Rev Entomol 42:525–55010.1146/annurev.ento.42.1.525 ↗
31. Lewinski N, Colvin V, Drezek R (2008) Cytotoxicity of nanoparticles. Small 4:26–4910.1002/smll.200700595 ↗
32. Li Y, Fetchko M, Lai ZC, Baker NE (2003) Scabrous and Gp150 are endosomal proteins that regulate Notch activity. Development 130:2819–282710.1242/dev.00495 ↗
33. Liang J, Deng Z, Jiang X, Li F, Li Y (2002) Photoluminescence of tetragonal ZrO2 nanoparticles synthesized by microwave irradiation. Inorg Chem 41:3602–360410.1021/ic025532q ↗
34. 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 19:780–78510.1111/j.1600-0501.2008.01524.x ↗
35. 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 40:4346–435210.1021/es060589n ↗
36. Lynch I, Dawson KA (2008) Protein-nanoparticle interactions. Nano Today 3:40–4710.1016/S1748-0132(08)70014-8 ↗
37. Manicone PF, Iommetti PR, Raffaelli L (2007) An overview of zirconia ceramics: basic properties and clinical applications. J Dent 35:819–82610.1016/j.jdent.2007.07.008 ↗
38. 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 67:778–79110.1002/dneu.20388 ↗
39. 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 3:7529–753710.1039/C5TB00832H ↗
40. 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 4:4420–442910.1039/C6TB01102K ↗
41. Nichols CD, Becnel J, Pandey UB (2012) Methods to assay Drosophila behavior. JoVE (J Vis Exp) e3795
42. Ohlstein B, Spradling A (2006) The adult Drosophila posterior midgut is maintained by pluripotent stem cells. Nature 439:470–47410.1038/nature04333 ↗
43. 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: 13610.1007/s11051-017-3824-8 ↗
44. Piconi C, Maccauro G (1999) Zirconia as a ceramic biomaterial. Biomaterials 20:1–2510.1016/S0142-9612(98)00010-6 ↗
45. 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 85:34–4210.1016/j.chemosphere.2011.06.040 ↗
46. 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 167:76–8510.1016/j.physbeh.2016.08.032 ↗
47. 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 2:2–610.4081/ams.2012.e2 ↗
48. 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 84:550–55810.1002/jbm.b.30903 ↗
49. 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 104:5199–520410.1073/pnas.0700895104 ↗
50. 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 28:340–34510.1590/S0102-86502013000500004 ↗
51. 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 3:7300–730610.1039/C5TB01424G ↗
52. Takashima S, Hartenstein V (2012) Genetic control of intestinal stem cell specification and development: a comparative view. Stem Cell Rev 8:597–60810.1007/s12015-012-9351-1 ↗
53. Tang S, Huang X, Chen X, Zheng N (2010) Hollow mesoporous zirconia nanocapsules for drug delivery. Adv Funct Mater 20:2442–244710.1002/adfm.201000647 ↗
54. Tsakonas A, Rand S, Matthew D, Lake JR (1999) Notch signaling: cell fate control and signal integration in development. Science 284:770–77610.1126/science.284.5415.770 ↗
55. 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 9:558–56910.1016/j.nano.2012.10.010 ↗
56. Wolff T, Ready DF (1991) Cell death in normal and rough eye mutants of Drosophila. Development 113:825–83910.1242/dev.113.3.825 ↗
57. 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 139:325–33410.1242/dev.074260 ↗
58. 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:e0329310.7554/eLife.03293 ↗