Silver nanoparticles disrupt germline stem cell maintenance in the Drosophila testis

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Ong, Cynthia ^a   Lee, Qian Ying ^a   Cai, Yu ^b   Liu, Xiaoli ^b   Ding, Jun ^b   Yung, Lin Yue Lanry ^b   Bay, Boon Huat ^a   Baeg, Gyeong Hun ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

METAL NANOPARTICLE; REACTIVE OXYGEN METABOLITE; SILVER;

ANIMAL; CELL DIFFERENTIATION; CELL SURVIVAL; CHEMISTRY; CYTOLOGY; DOSE RESPONSE; DROSOPHILA; DRUG EFFECTS; FERTILITY; GERM CELL; GROWTH, DEVELOPMENT AND AGING; MALE; METABOLISM; TESTIS;

ANIMALS; CELL DIFFERENTIATION; CELL SURVIVAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DROSOPHILA; FERTILITY; GERM CELLS; MALE; METAL NANOPARTICLES; REACTIVE OXYGEN SPECIES; SILVER; TESTIS;

EID: 84957606459     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep20632     Document Type: Article

References (56)

1. Oberdorster, G., Oberdorster, E., & Oberdorster, J. Nanotoxicology: an emerging discipline evolving from studies of ultrafine particles. Environ Health Perspect. 113, 823-839 (2005).
2. Lanone, S., & Boczkowski, J. Biomedical applications and potential health risks of nanomaterials: molecular mechanisms. Curr Mol Med. 6, 651-663 (2006).
3. Johnston, H. J., et al. A review of the in vivo and in vitro toxicity of silver and gold particulates: particle attributes and biological mechanisms responsible for the observed toxicity. Crit Rev Toxicol. 40, 328-346 (2010).
4. Liu, Y., Miyoshi, H., & Nakamura, M. Nanomedicine for drug delivery and imaging: a promising avenue for cancer therapy and diagnosis using targeted functional nanoparticles. Int J Cancer. 120, 2527-2537 (2007).
5. Eby, D. M., Luckarift, H. R., & Johnson, G. R. Hybrid antimicrobial enzyme and silver nanoparticle coatings for medical instruments. ACS Appl Mater Interfaces. 1, 1553-1560 (2009).
6. Pollini, M., et al. Antibacterial coatings on haemodialysis catheters by photochemical deposition of silver nanoparticles. J Mater Sci Mater Med. 22, 2005-2012 (2011).
7. Yee, W., Selvaduray, G., & Hawkins, B. Characterization of silver nanoparticle-infused tissue adhesive for ophthalmic use. J Mech Behav Biomed Mater. 55, 67-74 (2015).
8. AshaRani, P. V., Low Kah Mun, G., Hande, M. P., & Valiyaveettil, S. Cytotoxicity and genotoxicity of silver nanoparticles in human cells. ACS Nano. 3, 279-290 (2009).
9. Piao, M. J., et al. Silver nanoparticles induce oxidative cell damage in human liver cells through inhibition of reduced glutathione and induction of mitochondria-involved apoptosis. Toxicol Lett. 201, 92-100 (2011).
10. Loeschner, K., et al. Distribution of silver in rats following 28 days of repeated oral exposure to silver nanoparticles or silver acetate. Part Fibre Toxicol. 8, 18 (2011).
11. Braydich-Stolle, L. K., et al. Silver nanoparticles disrupt GDNF/Fyn kinase signaling in spermatogonial stem cells. Toxicol Sci. 116, 577-589 (2010).
12. Miresmaeili, S. M., et al. Evaluating the role of silver nanoparticles on acrosomal reaction and spermatogenic cells in rat. Iran J Reprod Med. 11, 423-430 (2013).
13. Mathias, F. T., et al. Daily exposure to silver nanoparticles during prepubertal development decreases adult sperm and reproductive parameters. Nanotoxicology (2014).
14. Han, J. W., et al. Male-And female-Derived somatic and germ cell-specific toxicity of silver nanoparticles in mouse. Nanotoxicology, 1-13 (2015).
15. de Cuevas, M., & Matunis, E. L. The stem cell niche: lessons from the Drosophila testis. Development. 138, 2861-2869 (2011).
16. Stocker, H., & Gallant, P. In Drosophila Vol. 420 Methods in Molecular Biology (ed Christian Dahmann) Ch. 2, 27-44 (Humana Press, 2008).
17. Pandey, U. B., & Nichols, C. D. Human disease models in Drosophila melanogaster and the role of the fly in therapeutic drug discovery. Pharmacol Rev. 63, 411-436 (2011).
18. Vecchio, G. A fruit fly in the nanoworld: once again Drosophila contributes to environment and human health. Nanotoxicology. 9, 135-137 (2015).
19. Ong, C., Yung, L. Y., Cai, Y., Bay, B. H., & Baeg, G. H. Drosophila melanogaster as a model organism to study nanotoxicity. Nanotoxicology. 9, 396-403 (2015).
20. Gorth, D. J., Rand, D. M., & Webster, T. J. Silver nanoparticle toxicity in Drosophila: size does matter. Int J Nanomedicine. 6, 343-350 (2011).
21. Armstrong, N., Ramamoorthy, M., Lyon, D., Jones, K., & Duttaroy, A. Mechanism of silver nanoparticles action on insect pigmentation reveals intervention of copper homeostasis. PLoS One. 8, e53186 (2013).
22. Key, S. C. S., Reaves, D., Turner, F., & Bang, J. J. Impacts of silver nanoparticle ingestion on pigmentation and developmental progression in Drosophila. Atlas J Biol. 1, 52-61 (2011).
23. Panacek, A., et al. Acute and chronic toxicity effects of silver nanoparticles (NPs) on Drosophila melanogaster. Environ Sci Technol. 45, 4974-4979 (2011).
24. Posgai, R., et al. 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 (2011).
25. Tian, H., et al. Development of biomarker for detecting silver nanoparticles exposure using a GAL4 enhancer trap screening in Drosophila. Environ Toxicol Pharmacol. 36, 548-556 (2013).
26. Han, X., et al. Monitoring the developmental impact of copper and silver nanoparticle exposure in Drosophila and their microbiomes. Sci Total Environ. 487, 822-829 (2014).
27. Avalos, A., Haza, A. I., Drosopoulou, E., Mavragani-Tsipidou, P., & Morales, P. In vivo genotoxicity assesment of silver nanoparticles of different sizes by the Somatic Mutation and Recombination Test (SMART) on Drosophila. Food Chem Toxicol. 85, 114-119 (2015).
28. Gromadzka-Ostrowska, J., et al. Silver nanoparticles effects on epididymal sperm in rats. Toxicol Lett. 214, 251-258 (2012).
29. Gonczy, P., Viswanathan, S., & DiNardo, S. Probing spermatogenesis in Drosophila with P-Element enhancer detectors. Development. 114, 89-98 (1992).
30. Voog, J., D?Alterio, C., & Jones, D. L. Multipotent somatic stem cells contribute to the stem cell niche in the Drosophila testis. Nature. 454, 1132-1136 (2008).
31. Spradling, A., Fuller, M. T., Braun, R. E., & Yoshida, S. Germline stem cells. Cold Spring Harb Perspect Biol. 3, a002642 (2011).
32. Hardy, R. W., Tokuyasu, K. T., Lindsley, D. L., & Garavito, M. The germinal proliferation center in the testis of Drosophila melanogaster. J Ultrastruct Res. 69, 180-190 (1979).
33. Ahamed, M., et al. Silver nanoparticles induced heat shock protein 70, oxidative stress and apoptosis in Drosophila melanogaster. Toxicol Appl Pharmacol. 242, 263-269 (2010).
34. Ebabe Elle, R., et al. Dietary exposure to silver nanoparticles in Sprague-Dawley rats: effects on oxidative stress and inflammation. Food Chem Toxicol. 60, 297-301 (2013).
35. Avalos, A., Haza, A. I., Mateo, D., & Morales, P. Cytotoxicity and ROS production of manufactured silver nanoparticles of different sizes in hepatoma and leukemia cells. J Appl Toxicol. 34, 413-423 (2014).
36. Pasqualotto, F. F., Sharma, R. K., Nelson, D. R., Thomas, A. J., & Agarwal, A. Relationship between oxidative stress, semen characteristics, and clinical diagnosis in men undergoing infertility investigation. Fertil Steril. 73, 459-464 (2000).
37. Nandipati, K. C., Pasqualotto, F. F., Thomas, A. J., Jr., & Agarwal, A. Relationship of interleukin-6 with semen characteristics and oxidative stress in vasectomy reversal patients. Andrologia. 37, 131-134 (2005).
38. Kalyanaraman, B., et al. Measuring reactive oxygen and nitrogen species with fluorescent probes: challenges and limitations. Free Radic Biol Med. 52, 1-6 (2012).
39. Sykiotis, G. P., & Bohmann, D. Keap1/Nrf2 signaling regulates oxidative stress tolerance and lifespan in Drosophila. Dev Cell. 14, 76-85 (2008).
40. Itoh, K., et al. An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem Biophys Res Commun. 236, 313-322 (1997).
41. Itoh, K., Tong, K. I., & Yamamoto, M. Molecular mechanism activating Nrf2-Keap1 pathway in regulation of adaptive response to electrophiles. Free Radic Biol Med. 36, 1208-1213 (2004).
42. Shi, X., Zhang, Y., Zheng, J., & Pan, J. Reactive oxygen species in cancer stem cells. Antioxid Redox Signal. 16, 1215-1228 (2012).
43. Liang, R., & Ghaffari, S. Stem cells, redox signaling, and stem cell aging. Antioxid Redox Signal. 20, 1902-1916 (2014).
44. Naka, K., Muraguchi, T., Hoshii, T., & Hirao, A. Regulation of reactive oxygen species and genomic stability in hematopoietic stem cells. Antioxid Redox Signal. 10, 1883-1894 (2008).
45. Ludin, A., et al. Reactive oxygen species regulate hematopoietic stem cell self-renewal, migration and development, as well as their bone marrow microenvironment. Antioxid Redox Signal. 21, 1605-1619 (2014).
46. Paik, J. H., et al. FoxOs cooperatively regulate diverse pathways governing neural stem cell homeostasis. Cell Stem Cell. 5, 540-553 (2009).
47. Owusu-Ansah, E., & Banerjee, U. Reactive oxygen species prime Drosophila haematopoietic progenitors for differentiation. Nature. 461, 537-541 (2009).
48. McKearin, D. M., & Spradling, A. C. bag-of-marbles: a Drosophila gene required to initiate both male and female gametogenesis. Genes Dev. 4, 2242-2251 (1990).
49. Gonczy, P., Matunis, E., & DiNardo, S. bag-of-marbles and benign gonial cell neoplasm act in the germline to restrict proliferation during Drosophila spermatogenesis. Development. 124, 4361-4371 (1997).
50. Insco, M. L., Leon, A., Tam, C. H., McKearin, D. M., & Fuller, M. T. Accumulation of a differentiation regulator specifies transit amplifying division number in an adult stem cell lineage. Proc Natl Acad Sci US A 106, 22311-22316 (2009).
51. Hime, G. R., Brill, J. A., & Fuller, M. T. Assembly of ring canals in the male germ line from structural components of the contractile ring. J Cell Sci. 109 (Pt 12), 2779-2788 (1996).
52. Fuller, M. T. Genetic control of cell proliferation and differentiation in Drosophila spermatogenesis. Semin Cell Dev Biol. 9, 433-444 (1998).
53. Davies, E. L., & Fuller, M. T. Regulation of self-renewal and differentiation in adult stem cell lineages: lessons from the Drosophila male germ line. Cold Spring Harb Symp Quant Biol. 73, 137-145 (2008).
54. Tran, J., Brenner, T. J., & DiNardo, S. Somatic control over the germline stem cell lineage during Drosophila spermatogenesis. Nature. 407, 754-757 (2000).
55. Castellini, C., et al. Long-Term effects of silver nanoparticles on reproductive activity of rabbit buck. Syst Biol Reprod Med. 60, 143-150 (2014).
56. Chen, D., & McKearin, D. M. A discrete transcriptional silencer in the bam gene determines asymmetric division of the Drosophila germline stem cell. Development. 130, 1159-1170 (2003).