Silver nanoparticles induced RNA polymerase-silver binding and RNA transcription inhibition in erythroid progenitor cells

ACS Nano

Volumn 7, Issue 5, 2013, Pages 4171-4186

  Wang, Zhe ^a   Liu, Sijin ^a   Ma, Juan ^a   Qu, Guangbo ^a   Wang, Xiaoyan ^a   Yu, Sujuan ^a   He, Jiuyang ^b   Liu, Jingfu ^a   Xia, Tian ^c   Jiang, Gui Bin ^a  

^a RESEARCH CENTER FOR ECO ENVIRONMENTAL SCIENCES   (China)

^b Tufts University   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

erythroid cells; nanosilver; RNA polymerase; transcription; trojan horse

Indexed keywords

ANTI-MICROBIAL ACTIVITY; ANTI-MICROBIAL PROPERTIES; BIOLOGICAL INFLUENCES; ERYTHROID CELLS; HEMOGLOBIN CONCENTRATION; NANO SILVER; RNA POLYMERASE; TROJAN HORSE;

BIOCHEMISTRY; CELLS; CYTOLOGY; HEMOGLOBIN; IONS; NANOPARTICLES; POLYMERS; RNA; TOXICITY; TRANSCRIPTION;

SILVER;

DNA DIRECTED RNA POLYMERASE; METAL NANOPARTICLE; SILVER;

ANIMAL; ARTICLE; CELL PROLIFERATION; CELL STRAIN HEPG2; CELL SURVIVAL; CHEMISTRY; CYTOLOGY; DOSE RESPONSE; DRUG EFFECT; ERYTHROID PRECURSOR CELL; GENETIC TRANSCRIPTION; HUMAN; METABOLISM; MOUSE; PROTEIN BINDING;

ANIMALS; CELL PROLIFERATION; CELL SURVIVAL; DNA-DIRECTED RNA POLYMERASES; DOSE-RESPONSE RELATIONSHIP, DRUG; ERYTHROID PRECURSOR CELLS; HEP G2 CELLS; HUMANS; METAL NANOPARTICLES; MICE; PROTEIN BINDING; SILVER; TRANSCRIPTION, GENETIC;

EID: 84878334606     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn400594s     Document Type: Article

References (79)

1. Sintubin, L.; Verstraete, W.; Boon, N. Biologically Produced Nanosilver: Current State and Future Perspectives Biotechnol. Bioeng. 2012, 109, 2422-2436
2. An Inventory of Nanotechnology-Based Consumer Products Currently on the Market. http://www.nanotechproject.org/inventories/consumer/analysis-draft/.
3. Morones, J. R.; Elechiguerra, J. L.; Camacho, A.; Holt, K.; Kouri, J. B.; Ramirez, J. T.; Yacaman, M. J. The Bactericidal Effect of Silver Nanoparticles Nanotechnology 2005, 16, 2346-2353
4. Shahverdi, A. R.; Fakhimi, A.; Shahverdi, H. R.; Minaian, S. Synthesis and Effect of Silver Nanoparticles on the Antibacterial Activity of Different Antibiotics against Staphylococcus aureus and Escherichia coli Nanomedicine 2007, 3, 168-171
5. Lu, L.; Sun, R. W.; Chen, R.; Hui, C. K.; Ho, C. M.; Luk, J. M.; Lau, G. K.; Che, C. M. Silver Nanoparticles Inhibit Hepatitis B Virus Replication Antiviral Ther. 2008, 13, 253-262
6. Maynard, A. D. Nanotechnology: A Research Strategy for Addressing Risk, Project on Emerging Nanotechnologies; Woodrow Wilson International Center for Scholars: Washington, DC, 2006; pp 1-41.
7. Chaloupka, K.; Malam, Y.; Seifalian, A. M. Nanosilver as a New Generation of Nanoproduct in Biomedical Applications Trends Biotechnol. 2010, 28, 580-588
8. Wijnhoven, S. W. P.; Peijnenburg, W. J. G. M.; Herberts, C. A.; Hagens, W. I.; Oomen, A. G.; Heugens, E. H. W.; Roszek, B.; Bisschops, J.; Gosens, I.; Van de Meent, D. Nano-Silver-a Review of Available Data and Knowledge Gaps in Human and Environmental Risk Assessment Nanotoxicology 2009, 3, 109-138
9. Christensen, F. M.; Johnston, H. J.; Stone, V.; Aitken, R. J.; Hankin, S.; Peters, S.; Aschberger, K. Nano-Silver-Feasibility and Challenges for Human Health Risk Assessment Based on Open Literature Nanotoxicology 2010, 4, 284-295
10. Fabrega, J.; Luoma, S. N.; Tyler, C. R.; Galloway, T. S.; Lead, J. R. Silver Nanoparticles: Behaviour and Effects in the Aquatic Environment Environ. Int. 2011, 37, 517-531
11. Varner, K.; Sanford, J. State of the Science Literature Review: Everything About Nanosilver and More; U.S. Environmental Protection Agency: Washington, DC, 2010.
12. Luoma, S. N. Silver Nanotechnologies and the Environment: Old Problems or New Challenges, Project on Emerging Nanotechnologies; The Pew Charitable Trusts: Washington, DC, 2008.
13. Yang, W.; Shen, C.; Ji, Q.; An, H.; Wang, J.; Liu, Q.; Zhang, Z. Food Storage Material Silver Nanoparticles Interfere with DNA Replication Fidelity and Bind with DNA Nanotechnology 2009, 20, 085102
14. Asharani, P. V.; Hande, M. P.; Valiyaveettil, S. Anti-Proliferative Activity of Silver Nanoparticles BMC Cell Biol. 2009, 10, 65
15. Hackenberg, S.; Scherzed, A.; Kessler, M.; Hummel, S.; Technau, A.; Froelich, K.; Ginzkey, C.; Koehler, C.; Hagen, R.; Kleinsasser, N. Silver Nanoparticles: Evaluation of DNA Damage, Toxicity and Functional Impairment in Human Mesenchymal Stem Cells Toxicol. Lett. 2011, 201, 27-33
16. AshaRani, P. V.; Low Kah Mun, G.; Hande, M. P.; Valiyaveettil, S. Cytotoxicity and Genotoxicity of Silver Nanoparticles in Human Cells ACS Nano 2009, 3, 279-290
17. Bar-Ilan, O.; Albrecht, R. M.; Fako, V. E.; Furgeson, D. Y. Toxicity Assessments of Multisized Gold and Silver Nanoparticles in Zebrafish Embryos Small 2009, 5, 1897-1910
18. Pratsinis, A.; Hervella, P.; Leroux, J. C.; Pratsinis, S. E.; Sotiriou, G. A. Toxicity of Silver Nanoparticles in Macrophages. Small 2013, in press.
19. Elnitski, L.; Hardison, R. Efficient and Reliable Transfection of Mouse Erythroleukemia Cells Using Cationic Lipids Blood Cell Mol. Dis. 1999, 25, 299-304
20. George, S.; Lin, S.; Ji, Z.; Thomas, C. R.; Li, L.; Mecklenburg, M.; Meng, H.; Wang, X.; Zhang, H.; Xia, T. Surface Defects on Plate-Shaped Silver Nanoparticles Contribute to Its Hazard Potential in a Fish Gill Cell Line and Zebrafish Embryos ACS Nano 2012, 6, 3745-3759
21. Zhao, C. M.; Wang, W. X. Size-Dependent Uptake of Silver Nanoparticles in Daphnia magna Environ. Sci. Technol. 2012, 46, 11345-11351
22. Liu, S.; Bhattacharya, S.; Han, A.; Suragani, R. N.; Zhao, W.; Fry, R. C.; Chen, J. J. Haem-Regulated Eif2alpha Kinase Is Necessary for Adaptive Gene Expression in Erythroid Precursors under the Stress of Iron Deficiency Br. J. Hamaetol. 2008, 143, 129-137
23. Hurwitz, J. The Discovery of RNA Polymerase J. Biol. Chem. 2005, 280, 42477-42485
24. Zhang, P.; Ma, Y.; Zhang, Z.; He, X.; Zhang, J.; Guo, Z.; Tai, R.; Zhao, Y.; Chai, Z. Biotransformation of Ceria Nanoparticles in Cucumber Plants ACS Nano 2012, 6, 9943-9950
25. Liu, J.; Wang, Z.; Liu, F. D.; Kane, A. B.; Hurt, R. H. Chemical Transformations of Nanosilver in Biological Environments ACS Nano 2012, 6, 9887-9899
26. Glover, R. D.; Miller, J. M.; Hutchison, J. E. Generation of Metal Nanoparticles from Silver and Copper Objects: Nanoparticle Dynamics on Surfaces and Potential Sources of Nanoparticles in the Environment ACS Nano 2011, 5, 8950-8957
27. Singh, M. P.; Atkins, T. M.; Muthuswamy, E.; Kamali, S.; Tu, C.; Louie, A. Y.; Kauzlarich, S. M. Development of Iron-Doped Silicon Nanoparticles as Bimodal Imaging Agents ACS Nano 2012, 6, 5596-5604
28. Mullick Chowdhury, S.; Lalwani, G.; Zhang, K.; Yang, J. Y.; Neville, K.; Sitharaman, B. Cell Specific Cytotoxicity and Uptake of Graphene Nanoribbons Biomaterials 2013, 34, 283-293
29. Yu, S. J.; Chao, J. B.; Sun, J.; Yin, Y. G.; Liu, J. F.; Jiang, G. B. Quantification of the Uptake of Silver Nanoparticles and Ions to Hepg2 Cells. Environ. Sci. Technol. 2013, in press.
30. Sotiriou, G. A.; Pratsinis, S. E. Antibacterial Activity of Nanosilver Ions and Particles Environ. Sci. Technol. 2010, 44, 5649-5654
31. Wang, Z.; Chen, J.; Li, X.; Shao, J.; Peijnenburg, W. J. Aquatic Toxicity of Nanosilver Colloids to Different Trophic Organisms: Contributions of Particles and Free Silver Ion Environ. Toxicol. Chem. 2012, 31, 2408-2413
32. Singh, S.; Nalwa, H. S. Nanotechnology and Health Safety-Toxicity and Risk Assessments of Nanostructured Materials on Human Health J. Nanosci. Nanotechnol. 2007, 7, 3048-3070
33. Limbach, L. K.; Wick, P.; Manser, P.; Grass, R. N.; Bruinink, A.; Stark, W. J. Exposure of Engineered Nanoparticles to Human Lung Epithelial Cells: Influence of Chemical Composition and Catalytic Activity on Oxidative Stress Environ. Sci. Technol. 2007, 41, 4158-4163
34. Xia, T.; Kovochich, M.; Liong, M.; Madler, L.; Gilbert, B.; Shi, H.; Yeh, J. I.; Zink, J. I.; Nel, A. E. Comparison of the Mechanism of Toxicity of Zinc Oxide and Cerium Oxide Nanoparticles Based on Dissolution and Oxidative Stress Properties ACS Nano 2008, 2, 2121-2134
35. Gunawan, C.; Teoh, W. Y.; Marquis, C. P.; Amal, R. Cytotoxic Origin of Copper(II) Oxide Nanoparticles: Comparative Studies with Micron-Sized Particles, Leachate, and Metal Salts ACS Nano 2011, 5, 7214-7225
36. Studer, A. M.; Limbach, L. K.; Van Duc, L.; Krumeich, F.; Athanassiou, E. K.; Gerber, L. C.; Moch, H.; Stark, W. J. Nanoparticle Cytotoxicity Depends on Intracellular Solubility: Comparison of Stabilized Copper Metal and Degradable Copper Oxide Nanoparticles Toxicol. Lett. 2010, 197, 169-174
37. Horie, M.; Nishio, K.; Fujita, K.; Kato, H.; Nakamura, A.; Kinugasa, S.; Endoh, S.; Miyauchi, A.; Yamamoto, K.; Murayama, H. Ultrafine Nio Particles Induce Cytotoxicity in Vitro by Cellular Uptake and Subsequent Ni(II) Release Chem. Res. Toxicol. 2009, 22, 1415-1426
38. Park, E. J.; Yi, J.; Kim, Y.; Choi, K.; Park, K. Silver Nanoparticles Induce Cytotoxicity by a Trojan-Horse Type Mechanism Toxicol. In Vitro 2010, 24, 872-878
39. Cronholm, P.; Karlsson, H. L.; Hedberg, J.; Lowe, T. A.; Winnberg, L.; Elihn, K.; Wallinder, I. O.; Möller, L. Intracellular Uptake and Toxicity of Ag and CuO Nanoparticles: A Comparison between Nanoparticles and Their Corresponding Metal Ions Small 2013, 9, 970-982
40. Havelaar, A. C.; de Gast, I. L.; Snijders, S.; Beerens, C. E.; Mancini, G. M.; Verheijen, F. W. Characterization of a Heavy Metal Ion Transporter in the Lysosomal Membrane FEBS Lett. 1998, 436, 223-227
41. Bury, N. R.; Grosell, M.; Grover, A. K.; Wood, C. M. ATP-Dependent Silver Transport across the Basolateral Membrane of Rainbow Trout Gills Toxicol. Appl. Pharmacol. 1999, 159, 1-8
42. Chopra, I. Bacterial RNA Polymerase: A Promising Target for the Discovery of New Antimicrobial Agents Curr. Opin. Invest. Drugs 2007, 8, 600-607
43. Yamada, K.; Koyama, H.; Hagiwara, K.; Ueda, A.; Sasaki, Y.; Kanesashi, S. N.; Ueno, R.; Nakamura, H. K.; Kuwata, K.; Shimizu, K. Identification of a Novel Compound with Antiviral Activity against Influenza a Virus Depending on Pa Subunit of Viral RNA Polymerase Microbes Infect. 2012, 14, 740-747
44. Floss, H. G.; Yu, T. W. Rifamycin-Mode of Action, Resistance, and Biosynthesis Chem. Rev. 2005, 105, 621-632
45. Wang, Z.; Qu, G.; Su, L.; Liu, S.; Jiang, G. Evaluation of the Biological Fate and the Transport through Biological Barriers of Nanosilver in Mice. Curr. Pharm. Des. 2013, in press.
46. Zhang, J.; Socolovsky, M.; Gross, A. W.; Lodish, H. F. Role of Ras Signaling in Erythroid Differentiation of Mouse Fetal Liver Cells: Functional Analysis by a Flow Cytometry-Based Novel Culture System Blood 2003, 102, 3938-3946
47. Nair, P. M.; Park, S. Y.; Lee, S. W.; Choi, J. Differential Expression of Ribosomal Protein Gene, Gonadotrophin Releasing Hormone Gene and Balbiani Ring Protein Gene in Silver Nanoparticles Exposed Chironomus riparius Aquat. Toxicol. 2011, 101, 31-37
48. Lee, K. J.; Nallathamby, P. D.; Browning, L. M.; Osgood, C. J.; Xu, X. H. In Vivo Imaging of Transport and Biocompatibility of Single Silver Nanoparticles in Early Development of Zebrafish Embryos ACS Nano 2007, 1, 133-143
49. Welch, J. J.; Watts, J. A.; Vakoc, C. R.; Yao, Y.; Wang, H.; Hardison, R. C.; Blobel, G. A.; Chodosh, L. A.; Weiss, M. J. Global Regulation of Erythroid Gene Expression by Transcription Factor Gata-1 Blood 2004, 104, 3136-3147
50. Griffitt, R. J.; Hyndman, K.; Denslow, N. D.; Barber, D. S. Comparison of Molecular and Histological Changes in Zebrafish Gills Exposed to Metallic Nanoparticles Toxicol. Sci. 2009, 107, 404-415
51. Pietroiusti, A.; Massimiani, M.; Fenoglio, I.; Colonna, M.; Valentini, F.; Palleschi, G.; Camaioni, A.; Magrini, A.; Siracusa, G.; Bergamaschi, A. Low Doses of Pristine and Oxidized Single-Wall Carbon Nanotubes Affect Mammalian Embryonic Development ACS Nano 2011, 5, 4624-4633
52. Yamashita, K.; Yoshioka, Y.; Higashisaka, K.; Mimura, K.; Morishita, Y.; Nozaki, M.; Yoshida, T.; Ogura, T.; Nabeshi, H.; Nagano, K. Silica and Titanium Dioxide Nanoparticles Cause Pregnancy Complications in Mice Nat. Nanotechnol. 2011, 6, 321-328
53. Chu, M.; Wu, Q.; Yang, H.; Yuan, R.; Hou, S.; Yang, Y.; Zou, Y.; Xu, S.; Xu, K.; Ji, A. Transfer of Quantum Dots from Pregnant Mice to Pups across the Placental Barrier Small 2010, 6, 670-678
54. Shimizu, M.; Tainaka, H.; Oba, T.; Mizuo, K.; Umezawa, M.; Takeda, K. Maternal Exposure to Nanoparticulate Titanium Dioxide During the Prenatal Period Alters Gene Expression Related to Brain Development in the Mouse Part. Fibre Toxicol. 2009, 6, 20
55. Hussain, S.; Boland, S.; Baeza-Squiban, A.; Hamel, R.; Thomassen, L. C.; Martens, J. A.; Billon-Galland, M. A.; Fleury-Feith, J.; Moisan, F.; Pairon, J. C. Oxidative Stress and Proinflammatory Effects of Carbon Black and Titanium Dioxide Nanoparticles: Role of Particle Surface Area and Internalized Amount Toxicology 2009, 260, 142-149
56. Lyon, T. D.; Patriarca, M.; Howatson, G.; Fleming, P. J.; Blair, P. S.; Fell, G. S. Age Dependence of Potentially Toxic Elements (Sb, Cd, Pb, Ag) in Human Liver Tissue from Paediatric Subjects J. Environ. Monit. 2002, 4, 1034-1039
57. Carlson, C.; Hussain, S. M.; Schrand, A. M.; Braydich-Stolle, L. K.; Hess, K. L.; Jones, R. L.; Schlager, J. J. Unique Cellular Interaction of Silver Nanoparticles: Size-Dependent Generation of Reactive Oxygen Species J. Phys. Chem. B 2008, 112, 13608-13619
58. Kim, S.; Choi, J. E.; Choi, J.; Chung, K. H.; Park, K.; Yi, J.; Ryu, D. Y. Oxidative Stress-Dependent Toxicity of Silver Nanoparticles in Human Hepatoma Cells Toxicol. In Vitro 2009, 23, 1076-1084
59. Boonstra, J.; Post, J. A. Molecular Events Associated with Reactive Oxygen Species and Cell Cycle Progression in Mammalian Cells Gene 2004, 337, 1-13
60. You, C.; Han, C.; Wang, X.; Zheng, Y.; Li, Q.; Hu, X.; Sun, H. The Progress of Silver Nanoparticles in the Antibacterial Mechanism, Clinical Application and Cytotoxicity Mol. Biol. Rep. 2012, 39, 9193-9201
61. Sotiriou, G. A.; Pratsinis, S. E. Antibacterial Activity of Nanosilver Ions and Particles Environ. Sci. Technol. 2010, 44, 5649-5654
62. Yamanaka, M.; Hara, K.; Kudo, J. Bactericidal Actions of a Silver Ion Solution on Escherichia coli, Studied by Energy-Filtering Transmission Electron Microscopy and Proteomic Analysis Appl. Environ. Microbiol. 2005, 71, 7589-7593
63. Bouwmeester, H.; Poortman, J.; Peters, R. J.; Wijma, E.; Kramer, E.; Makama, S.; Puspitaninganindita, K.; Marvin, H. J. P.; Peijnenburg, A. A. C. M.; Hendriksen, P. J. M. Characterization of Translocation of Silver Nanoparticles and Effects on Whole-Genome Gene Expression Using an in Vitro Intestinal Epithelium Coculture Model ACS Nano 2011, 5, 4091-4103
64. Liu, J. Y.; Sonshine, D. A.; Shervani, S.; Hurt, R. H. Controlled Release of Biologically Active Silver from Nanosilver Surfaces ACS Nano 2010, 4, 6903-6913
65. Liu, J.; Hurt, R. H. Ion Release Kinetics and Particle Persistence in Aqueous Nano-Silver Colloids Environ. Sci. Technol. 2010, 44, 2169-2175
66. Kawata, K.; Osawa, M.; Okabe, S. In Vitro Toxicity of Silver Nanoparticles at Noncytotoxic Doses to HepG2 Human Hepatoma Cells Environ. Sci. Technol. 2009, 43, 6046-6051
67. Laban, G.; Nies, L. F.; Turco, R. F.; Bickham, J. W.; Sepulveda, M. S. The Effects of Silver Nanoparticles on Fathead minnow (Pimephales promelas) Embryos Ecotoxicology 2010, 19, 185-195
68. Xiu, Z. M.; Zhang, Q. B.; Puppala, H. L.; Colvin, V. L.; Alvarez, P. J. Negligible Particle-Specific Antibacterial Activity of Silver Nanoparticles Nano Lett. 2012, 12, 4271-4275
69. Osborne, O. J.; Johnston, B. D.; Moger, J.; Balousha, M.; Lead, J. R.; Kudoh, T.; Tyler, C. R. Effects of Particle Size and Coating on Nanoscale Ag and Tio(2) Exposure in Zebrafish (Danio rerio) Embryos. Nanotoxicology 2012, in press.
70. Grosse, S.; Evje, L.; Syversen, T. Silver Nanoparticle-Induced Cytotoxicity in Rat Brain Endothelial Cell Culture Toxicol. In Vitro 2013, 27, 305-313
71. Levard, C.; Hotze, E. M.; Lowry, G. V.; Brown, G. E., Jr. Environmental Transformations of Silver Nanoparticles: Impact on Stability and Toxicity Environ. Sci. Technol. 2012, 46, 6900-6914
72. Lok, C. N.; Ho, C. M.; Chen, R.; He, Q. Y.; Yu, W. Y.; Sun, H.; Tam, P. K.; Chiu, J. F.; Che, C. M. Silver Nanoparticles: Partial Oxidation and Antibacterial Activities J. Biol. Inorg. Chem. 2007, 12, 527-534
73. Romanova, L.; Grand, A.; Zhang, L.; Rayner, S.; Katoku-Kikyo, N.; Kellner, S.; Kikyo, N. Critical Role of Nucleostemin in Pre-rRNA Processing J. Biol. Chem. 2009, 284, 4968-4977
74. Liu, S.; Suragani, R. N.; Wang, F.; Han, A.; Zhao, W.; Andrews, N. C.; Chen, J. J. The Function of Heme-Regulated Eif2alpha Kinase in Murine Iron Homeostasis and Macrophage Maturation J. Clin. Invest. 2007, 117, 3296-3305
75. Guang, S.; Bochner, A. F.; Burkhart, K. B.; Burton, N.; Pavelec, D. M.; Kennedy, S. Small Regulatory RNAs Inhibit RNA Polymerase II During the Elongation Phase of Transcription Nature 2010, 465, 1097-1101
76. Abmayr, S. M.; Yao, T.; Parmely, T.; Workman, J. L. Preparation of Nuclear and Cytoplasmic Extracts from Mammalian Cells. Curr. Protoc. Mol. Biol. 2006, Chapter 12, Unit 12 11.
77. Patterson, T. A.; Lobenhofer, E. K.; Fulmer-Smentek, S. B.; Collins, P. J.; Chu, T. M.; Bao, W. J.; Fang, H.; Kawasaki, E. S.; Hager, J.; Tikhonova, I. R. Performance Comparison of One-Color and Two-Color Platforms within the Microarray Quality Control (Maqc) Project Nat. Biotechnol. 2006, 24, 1140-1150
78. Liu, J. F.; Chao, J. B.; Liu, R.; Tan, Z. Q.; Yin, Y. G.; Wu, Y.; Jiang, G. B. Cloud Point Extraction as an Advantageous Preconcentration Approach for Analysis of Trace Silver Nanoparticles in Environmental Waters Anal. Chem. 2009, 81, 6496-6502
79. Prus, E.; Fibach, E. Flow Cytometry Measurement of the Labile Iron Pool in Human Hematopoietic Cells Cytometry, Part A 2008, 73, 22-27