Drosophila melanogaster as a model organism to study nanotoxicity

Nanotoxicology

Volumn 9, Issue 3, 2015, Pages 396-403

  Ong, Cynthia ^a   Yung, Lin Yue Lanry ^b   Cai, Yu ^b   Bay, Boon Huat ^a   Baeg, Gyeong Hun ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

Drosophila melanogaster; in vivo model organism; Nanomaterials; Toxicity

Indexed keywords

GOLD NANOPARTICLE; NANOMATERIAL; SILICA NANOPARTICLE; SILVER NANOPARTICLE; SINGLE WALLED NANOTUBE; TITANIUM DIOXIDE NANOPARTICLE; MUTAGENIC AGENT;

DNA DAMAGE; DNA FRAGMENTATION; DROSOPHILA MELANOGASTER; FERTILITY; FRUIT FLY MODEL; GENOTOXICITY; METABOLIC DISORDER; MITOTIC RECOMBINATION; MOLECULAR BIOLOGY; NANOTOXICOLOGY; NONHUMAN; OXIDATIVE STRESS; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; REVIEW; ANIMAL; ANIMAL MODEL; DRUG EFFECTS; GENETICS; METABOLISM;

ANIMALIA; DROSOPHILA MELANOGASTER; MAMMALIA; RODENTIA;

ANIMALS; DROSOPHILA MELANOGASTER; FERTILITY; MODELS, ANIMAL; MUTAGENS; NANOSTRUCTURES; OXIDATIVE STRESS;

EID: 84929663052     PISSN: 17435390     EISSN: 17435404     Source Type: Journal    
DOI: 10.3109/17435390.2014.940405     Document Type: Review

References (91)

1. Adams MD, Celniker SE, Holt RA, Evans CA, Gocayne JD, Amanatides PG, et al. 2000. The genome sequence of Drosophila melanogaster. Science 287:2185-95.
2. Adolfsson K, Schneider M, Hammarin G, Hacker U, Prinz CN. 2013. Ingestion of gallium phosphide nanowires has no adverse effect on Drosophila tissue function. Nanotechnology 24:285101.
3. 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: 263-9.
4. Ambalavanan N, Stanishevsky A, Bulger A, Halloran B, Steele C, Vohra Y, Matalon S. 2013. Titanium oxide nanoparticle instillation induces inflammation and inhibits lung development in mice. Am J Physiol Lung Cell Mol Physiol 304:L152-61.
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:e53186.
6. Auerbach C. 1947. Abnormal segregation after chemical treatment of Drosophila. Genetics 32:3-7.
7. Balasubramanian SK, Jittiwat J, Manikandan J, Ong CN, Yu LE, Ong WY. 2010. Biodistribution of gold nanoparticles and gene expression changes in the liver and spleen after intravenous administration in rats. Biomaterials 31:2034-42.
8. Barandeh F, Nguyen PL, Kumar R, Iacobucci GJ, Kuznicki ML, Kosterman A, et al. 2012. Organically modified silica nanoparticles are biocompatible and can be targeted to neurons in vivo. PLoS One 7: e29424.
9. Bellen HJ, Tong C, Tsuda H. 2010. 100 Years of Drosophila research and its impact on vertebrate neuroscience: a history lesson for the future. Nat Rev Neurosci 11:514-22.
10. Bhargav D, Pratap Singh M, Murthy RC, Mathur N, Misra D, Saxena DK, Kar Chowdhuri D. 2008. Toxic potential of municipal solid waste leachates in transgenic Drosophila melanogaster (hsp70-lacZ): hsp70 as a marker of cellular damage. Ecotoxicol Environ Saf 69: 233-45.
11. Brunetti V, Chibli H, Fiammengo R, Galeone A, Malvindi MA, Vecchio G, et al. 2013. InP/ZnS as a safer alternative to CdSe/ZnS core/shell quantum dots: in vitro and in vivo toxicity assessment. Nanoscale 5: 307-17.
12. Canavoso LE, Jouni ZE, Karnas KJ, Pennington JE, Wells MA. 2001. Fat metabolism in insects. Annu Rev Nutr 21:23-46.
13. Chen PH, Hsiao KM, Chou CC. 2013. Molecular characterization of toxicity mechanism of single-walled carbon nanotubes. Biomaterials 34:5661-9.
14. Coulom H, Birman S. 2004. Chronic exposure to rotenone models sporadic Parkinson's disease in Drosophila melanogaster. J Neurosci 24:10993-8.
15. De Andrade LR, Sandin Brito A, De Souza Melero AM, Zanin H, Jose Ceragioli H, Baranauskas V, et al. 2014. Absence of mutagenic and recombinagenic activity of multi-walled carbon nanotubes in the Drosophila wing-spot test and Allium cepa test. Ecotoxicol Environ Saf 99:92-7.
16. Dean BJ. 1985. Recent findings on the genetic toxicology of benzene, toluene, xylenes and phenols. Mutat Res 154:153-81.
17. 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 93:2304-10.
18. Demir E, Vales G, Kaya B, Creus A, Marcos R. 2011. Genotoxic analysis of silver nanoparticles in Drosophila. Nanotoxicology 5: 417-24.
19. Deshpande SA, Carvalho GB, Amador A, Phillips AM, Hoxha S, Lizotte KJ, Ja WW. 2014. Quantifying Drosophila food intake: comparative analysis of current methodology. Nat Methods 11:535-40.
20. Diangelo JR, Birnbaum MJ. 2009. Regulation of fat cell mass by insulin in Drosophila melanogaster. Mol Cell Biol 29:6341-52.
21. Duan J, Yu Y, Shi H, Tian L, Guo C, Huang P, et al. 2013. Toxic effects of silica nanoparticles on zebrafish embryos and larvae. PLoS One 8: e74606.
22. Eby DM, Luckarift HR, Johnson GR. 2009. Hybrid antimicrobial enzyme and silver nanoparticle coatings for medical instruments. ACS Appl Mater Interfaces 1:1553-60.
23. Fangueiro JF, Gonzalez-Mira E, Martins-Lopes P, Egea MA, Garcia ML, Souto SB, Souto EB. 2013. A novel lipid nanocarrier for insulin delivery: production, characterization and toxicity testing. Pharm Dev Technol 18:545-9.
24. Fuller MT, Spradling AC. 2007. Male and female Drosophila germline stem cells: two versions of immortality. Science 316:402-4.
25. Galeone A, Vecchio G, Malvindi MA, Brunetti V, Cingolani R, Pompa PP. 2012. In vivo assessment of CdSe-ZnS quantum dots: coating dependent bioaccumulation and genotoxicity. Nanoscale 4:6401-7.
26. Gorth DJ, Rand DM, Webster TJ. 2011. Silver nanoparticle toxicity in Drosophila: size does matter. Int J Nanomedicine 6:343-50.
27. Goyal R, Tripathi SK, Tyagi S, Ram KR, Ansari KM, Kumar P, et al. 2011. Gellan gum-PEI nanocomposites as efficient gene delivery agents. J Biomed Nanotechnol 7:38-9.
28. Graf U, Wurgler FE, Katz AJ, Frei H, Juon H, Hall CB, Kale PG. 1984. Somatic mutation and recombination test in Drosophila melanogaster. Environ Mutagen 6:153-88.
29. Greenspan RJ. 2004. Fly pushing: the theory and practice of Drosophila genetics. Cold Spring Harbor (NY): Cold Spring Harbor Laboratory Press.
30. Gupta SC, Siddique HR, Mathur N, Mishra RK, Saxena DK, Chowdhuri DK. 2007. Adverse effect of organophosphate compounds, dichlorvos and chlorpyrifos in the reproductive tissues of transgenic Drosophila melanogaster: 70 kDa heat shock protein as a marker of cellular damage. Toxicology 238:1-14.
31. Hemmati A, Scott K, Davis J. 2009. Nano analysis of silver nanoparticles in commercial socks. Microsc Microanal 15:552-3.
32. Hodgson E. 2004. Introduction to toxicology. A textbook of modern toxicology. Hoboken (NJ): John Wiley & Sons, Inc.
33. Hosamani R. 2013. Acute exposure of Drosophila melanogaster to paraquat causes oxidative stress and mitochondrial dysfunction. Arch Insect Biochem Physiol 83:25-40.
34. Huang N, Yan Y, Xu Y, Jin Y, Lei J, Zou X, et al. 2013. Alumina nanoparticles alter rhythmic activities of local interneurons in the antennal lobe of Drosophila. Nanotoxicology 7:212-20.
35. Jaeger A, Weiss DG, Jonas L, Kriehuber R. 2012. Oxidative stressinduced cytotoxic and genotoxic effects of nano-sized titanium dioxide particles in human HaCaT keratinocytes. Toxicology 296:27-36.
36. Jang S, Jang H, Lee Y, Suh D, Baik S, Hong BH, Ahn JH. 2010. Flexible, transparent single-walled carbon nanotube transistors with graphene electrodes. Nanotechnology 21:425201.
37. Key SCS, Reaves D, Turner F, Bang JJ. 2011. Impacts of silver nanoparticle ingestion on pigmentation and developmental progression in Drosophila. Atlas J Biol 1:52-61.
38. Kislukhin G, Murphy ML, Jafari M, Long AD. 2012. Chemotherapyinduced toxicity is highly heritable in Drosophila melanogaster. Pharmacogenet Genomics 22:285-9.
39. Lee Y, Kim P, Yoon J, Lee B, Choi K, Kil KH, Park K. 2013. Serum kinetics, distribution and excretion of silver in rabbits following 28 days after a single intravenous injection of silver nanoparticles. Nanotoxicology 7:1120-30.
40. Lehmann FO. 2001. Matching spiracle opening to metabolic need during flight in Drosophila. Science 294:1926-9.
41. Li JJ, Hartono D, Ong CN, Bay BH, Yung LYL. 2010a. Autophagy and oxidative stress associated with gold nanoparticles. Biomaterials 31: 5996-6003.
42. Li JJ, Lo SL, Ng CT, Gurung RL, Hartono D, Hande MP, et al. 2011. Genomic instability of gold nanoparticle treated human lung fibroblast cells. Biomaterials 32:5515-23.
43. Li JJ, Muralikrishnan S, Ng CT, Yung LYL, Bay BH. 2010b. Nanoparticle-induced pulmonary toxicity. Exp Biol Med (Maywood) 235:1025-33.
44. Li JJ, Zou L, Hartono D, Ong CN, Bay BH, Yung LYL. 2008. Gold nanoparticles induce oxidative damage in lung fibroblasts in vitro. Adv Mater 20:138-42.
45. Lim ZZ, Li JE, Ng CT, Yung LYL, Bay BH. 2011. Gold nanoparticles in cancer therapy. Acta Pharmacol Sin 32:983-90.
46. Lin KY, Kwong GA, Warren AD, Wood DK, Bhatia SN. 2013. Nanoparticles that sense thrombin activity as synthetic urinary biomarkers of thrombosis. ACS Nano 7:9001-9.
47. Lindberg HK, Falck GC, Singh R, Suhonen S, Jarventaus H, Vanhala E, et al. 2013. Genotoxicity of short single-wall and multi-wall carbon nanotubes in human bronchial epithelial and mesothelial cells in vitro. Toxicology 313:24-37.
48. Lindberg HK, Falck GCM, Suhonen S, Vippola M, Vanhala E, Catalan J, et al. 2009. Genotoxicity of nanomaterials: DNA damage and micronuclei induced by carbon nanotubes and graphite nanofibres in human bronchial epithelial cells in vitro. Toxicol Lett 186:166-173.
49. Liu X, Vinson D, Abt D, Hurt RH, Rand DM. 2009. Differential toxicity of carbon nanomaterials in Drosophila: larval dietary uptake is benign, but adult exposure causes locomotor impairment and mortality. Environ Sci Technol 43:6357-63.
50. Marcel V, Dichtel-Danjoy ML, Sagne C, Hafsi H, Ma D, Ortiz-Cuaran S, et al. 2011. Biological functions of p53 isoforms through evolution: lessons from animal and cellular models. Cell Death Differ 18: 1815-24.
51. Matsumoto H, Tanaka K, Noguchi H, Hayakawa Y. 2003. Cause of mortality in insects under severe stress. Eur J Biochem 270: 3469-76.
52. Morgan TH. 1910. Sex limited inheritance in Drosophila. Science 32: 120-2.
53. Muller HJ. 1928. The production of mutations by X-rays. Proc Natl Acad Sci USA 14:714-26.
54. Ng CT, Dheen ST, Yip WC, Ong CN, Bay BH, Yung LYL. 2011. The induction of epigenetic regulation of PROS1 gene in lung fibroblasts by gold nanoparticles and implications for potential lung injury. Biomaterials 32:7609-15.
55. Ng CT, Li JJ, Gurung RL, Hande MP, Ong CN, Bay BH, Yung LYL. 2013. Toxicological profile of small airway epithelial cells exposed to gold nanoparticles. Exp Biol Med (Maywood) 238:1355-61.
56. Ong C, Lim JZ, Ng CT, Li JJ, Yung LYL, Bay BH. 2013. Silver nanoparticles in cancer: therapeutic efficacy and toxicity. Curr Med Chem 20:772-81.
57. Panacek A, Prucek R, Safarova D, Dittrich M, Richtrova J, Benickova K, et al. 2011. Acute and chronic toxicity effects of silver nanoparticles (NPs) on Drosophila melanogaster. Environ Sci Technol 45:4974-9.
58. Panahifar A, Mahmoudi M, Doschak MR. 2013. Synthesis and in vitro evaluation of bone-seeking superparamagnetic iron oxide nanoparticles as contrast agents for imaging bone metabolic activity. ACS Appl Mater Interfaces 5:5219-26.
59. Pandey A, Chandra S, Chauhan LK, Narayan G, Chowdhuri DK. 2013. Cellular internalization and stress response of ingested amorphous silica nanoparticles in the midgut of Drosophila melanogaster. Biochim Biophys Acta 1830:2256-66.
60. Pandey UB, Nichols CD. 2011. Human disease models in Drosophila melanogaster and the role of the fly in therapeutic drug discovery. Pharmacol Rev 63:411-36.
61. Passagne I, Morille M, Rousset M, Pujalte I, L'azou B. 2012. Implication of oxidative stress in size-dependent toxicity of silica nanoparticles in kidney cells. Toxicology 299:112-24.
62. Paula MT, Zemolin AP, Vargas AP, Golombieski RM, Loreto EL, Saidelles AP, et al. 2012. Effects of Hg(II) exposure on MAPK phosphorylation and antioxidant system in D. melanogaster. Environ Toxicol 29:621-30.
63. Petkovic J, Zegura B, Stevanovic M, Drnovsek N, Uskokovic D, Novak S, Filipic M. 2011. DNA damage and alterations in expression of DNA damage responsive genes induced by TiO2 nanoparticles in human hepatoma HepG2 cells. Nanotoxicology 5:341-53.
64. Pfeiffer C, Rehbock C, Huhn D, Carrillo-Carrion C, De Aberasturi DJ, Merk V, Barcikowski S, Parak WJ. 2014. Interaction of colloidal nanoparticles with their local environment: the (ionic) nanoenvironment around nanoparticles is different from bulk and determines the physico-chemical properties of the nanoparticles. J R Soc Interface 11: 20130931.
65. Philbrook NA, Winn LM, Afrooz AR, Saleh NB, Walker VK. 2011. The effect of TiO(2) and Ag nanoparticles on reproduction and development of Drosophila melanogaster and CD-1 mice. Toxicol Appl Pharmacol 257:429-36.
66. Pichardo S, Gutierrez-Praena D, Puerto M, Sanchez E, Grilo A, Camean AM, Jos A. 2012. Oxidative stress responses to carboxylic acid functionalized single wall carbon nanotubes on the human intestinal cell line Caco-2. Toxicol In Vitro 26:672-7.
67. Pompa P, Vecchio G, Galeone A, Brunetti V, Sabella S, Maiorano G, et al. 2011a. In vivo toxicity assessment of gold nanoparticles in Drosophila melanogaster. Nano Research 4:405-13.
68. Pompa PP, Vecchio G, Galeone A, Brunetti V, Maiorano G, Sabella S, Cingolani R. 2011b. Physical assessment of toxicology at nanoscale: nano dose-metrics and toxicity factor. Nanoscale 3:2889-97.
69. Posgai R, Ahamed M, Hussain SM, Rowe JJ, Nielsen MG. 2009. Inhalation method for delivery of nanoparticles to the Drosophila respiratory system for toxicity testing. Sci Total Environ 408:439-43.
70. 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.
71. Powell MC, Kanarek MS. 2006a. Nanomaterial health effects-part 1: background and current knowledge. WMJ 105:16-20.
72. Powell MC, Kanarek MS. 2006b. Nanomaterial health effects-part 2: uncertainties and recommendations for the future. WMJ 105:18-23.
73. Rand MD. 2010. Drosophotoxicology: the growing potential for Drosophila in neurotoxicology. Neurotoxicol Teratol 32:74-83.
74. Reiter LT, Potocki L, Chien S, Gribskov M, Bier E. 2001. A systematic analysis of human disease-associated gene sequences in Drosophila melanogaster. Genome Res 11:1114-25.
75. Sayes CM, Wahi R, Kurian PA, Liu Y, West JL, Ausman KD, et al. 2006. Correlating nanoscale titania structure with toxicity: a cytotoxicity and inflammatory response study with human dermal fibroblasts and human lung epithelial cells. Toxicol Sci 92:174-85.
76. Scenir. (Scientific Committee on Emerging and Newly Identified Health Risks). Opinion on the scientific basis for the definition of the term ''nanomaterial''. European Comission, European Union 8 December, 2010.
77. Shukla RK, Sharma V, Pandey AK, Singh S, Sultana S, Dhawan A. 2011. ROS-mediated genotoxicity induced by titanium dioxide nanoparticles in human epidermal cells. Toxicol In Vitro 25:231-41.
78. Siddique YH, Fatima A, Jyoti S, Naz F, Rahul, Khan W, et al. 2013. Evaluation of the toxic potential of graphene copper nanocomposite (GCNC) in the third instar larvae of transgenic Drosophila melanogaster (hsp70-lacZ)Bg(9.). PLoS One 8:e80944.
79. Simon M, Barberet P, Delville MH, Moretto P, Seznec H. 2011. Titanium dioxide nanoparticles induced intracellular calcium homeostasis modification in primary human keratinocytes. Towards an in vitro explanation of titanium dioxide nanoparticles toxicity. Nanotoxicology 5:125-39.
80. Stefano HSD. 1943. Effects of silver nitrate on the pigmentation of Drosophila. Am Nat 77:94-6.
81. Stocker H, Gallant P. 2008. Getting started: an overview on raising and handling Drosophila. Methods Mol Biol 420:27-44.
82. Sykiotis GP, Bohmann D. 2008. Keap1/Nrf2 signaling regulates oxidative stress tolerance and lifespan in Drosophila. Dev Cell 14:76-85.
83. Tian H, Eom HJ, Moon S, Lee J, Choi J, Chung YD. 2013. Development of biomarker for detecting silver nanoparticles exposure using a GAL4 enhancer trap screening in Drosophila. Environ Toxicol Pharmacol 36: 548-56.
84. Tiwari AK, Pragya P, Ravi Ram K, Chowdhuri DK. 2011. Environmental chemical mediated male reproductive toxicity: Drosophila melanogaster as an alternate animal model. Theriogenology 76:197-216.
85. Tripp RA, Alvarez R, Anderson B, Jones L, Weeks C, Chen W. 2007. Bioconjugated nanoparticle detection of respiratory syncytial virus infection. Int J Nanomedicine 2:117-24.
86. Turrens JF. 2003. Mitochondrial formation of reactive oxygen species. J Physiol 552:335-44.
87. Vales G, Demir E, Kaya B, Creus A, Marcos R. 2013. Genotoxicity of cobalt nanoparticles and ions in Drosophila. Nanotoxicology 7:462-8.
88. Vecchio G. 2014. A fruit fly in the nanoworld: once again Drosophila contributes to environment and human health. Nanotoxicology. [Epub ahead of print]. doi: 10.3109/17435390.2014.911985.
89. Vecchio G, Galeone A, Brunetti V, Maiorano G, Rizzello L, Sabella S, et al. 2012a. Mutagenic effects of gold nanoparticles induce aberrant phenotypes in Drosophila melanogaster. Nanomedicine 8:1-7.
90. Vecchio G, Galeone A, Brunetti V, Maiorano G, Sabella S, Cingolani R, Pompa PP. 2012b. Concentration-dependent, size-independent toxicity of citrate capped AuNPs in Drosophila melanogaster. PLoS One 7: e29980.
91. Yu LE, Lanry Yung L-Y, Ong C-N, Tan Y-L, Suresh Balasubramaniam K, Hartono D, et al. 2007. Translocation and effects of gold nanoparticles after inhalation exposure in rats. Nanotoxicology 1:235-242.