Graphene oxide induces toll-like receptor 4 (TLR4)-dependent necrosis in macrophages

ACS Nano

Volumn 7, Issue 7, 2013, Pages 5732-5745

  Qu, Guangbo ^a   Liu, Sijin ^a   Zhang, Shuping ^a   Wang, Lei ^a   Wang, Xiaoyan ^a   Sun, Bingbing ^b   Yin, Nuoya ^a   Gao, Xiang ^c   Xia, Tian ^b   Chen, Jane Jane ^d   Jiang, Gui Bin ^a  

^a RESEARCH CENTER FOR ECO ENVIRONMENTAL SCIENCES   (China)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c NANJING UNIVERSITY   (China)

^d Massachusetts Institute of Technology Cambridge   (United States)

Author keywords

cytoskeleton; graphene; macrophages; necrosis; oxidative stress; toll like receptor 4

Indexed keywords

CYTOSKELETONS; MOLECULAR MECHANISM; NECROSIS; NECROTIC CELL DEATHS; OPTICAL CHARACTERISTICS; REACTIVE OXYGEN SPECIES; SELECTIVE INHIBITORS; TOLL-LIKE RECEPTOR 4;

ANTIGEN-ANTIBODY REACTIONS; CELL DEATH; GRAPHENE; NANOSTRUCTURED MATERIALS; OXIDATIVE STRESS; TOXICITY;

MACROPHAGES;

GRAPHITE; NANOPARTICLE; OXIDE;

ANIMAL; APOPTOSIS; ARTICLE; CELL LINE; CELL STRAIN HEK293; CHEMICALLY INDUCED DISORDER; DRUG EFFECT; HUMAN; MACROPHAGE; MATERIALS TESTING; MOUSE; NECROSIS; PATHOLOGY; CHEMICALLY INDUCED; DRUG EFFECTS; HEK293 CELL LINE;

ANIMALS; APOPTOSIS; CELL LINE; GRAPHITE; HEK293 CELLS; HUMANS; MACROPHAGES; MATERIALS TESTING; MICE; NANOPARTICLES; NECROSIS; OXIDES;

EID: 84880774116     PISSN: 19360851     EISSN: 1936086X     Source Type: Journal    
DOI: 10.1021/nn402330b     Document Type: Article

References (77)

1. Feng, L. Z.; Liu, Z. A. Graphene in Biomedicine: Opportunities and Challenges Nanomedicine 2011, 6, 317-324
2. Wang, Y. H.; Li, Z. H.; Wang, J.; Li, J. H.; Lin, Y. H. Graphene and Graphene Oxide: Biofunctionalization and Applications in Biotechnology Trends Biotechnol. 2011, 29, 205-212
3. Geim, A. K. Graphene: Status and Prospects Science 2009, 324, 1530-1534
4. Robinson, J. T.; Tabakman, S. M.; Liang, Y. Y.; Wang, H. L.; Casalongue, H. S.; Vinh, D.; Dai, H. J. Ultrasmall Reduced Graphene Oxide with High near-Infrared Absorbance for Photothermal Therapy J. Am. Chem. Soc. 2011, 133, 6825-6831
5. Sun, X. M.; Liu, Z.; Welsher, K.; Robinson, J. T.; Goodwin, A.; Zaric, S.; Dai, H. J. Nano-Graphene Oxide for Cellular Imaging and Drug Delivery Nano Res. 2008, 1, 203-212
6. Liu, Z.; Robinson, J. T.; Sun, X.; Dai, H. Pegylated Nanographene Oxide for Delivery of Water-Insoluble Cancer Drugs J. Am. Chem. Soc. 2008, 130, 10876-10877
7. Yang, K.; Zhang, S.; Zhang, G.; Sun, X.; Lee, S. T.; Liu, Z. Graphene in Mice: Ultrahigh in Vivo Tumor Uptake and Efficient Photothermal Therapy Nano Lett. 2010, 10, 3318-3323
8. Yang, K.; Wan, J. M.; Zhang, S. A.; Zhang, Y. J.; Lee, S. T.; Liu, Z. A. In Vivo Pharmacokinetics, Long-Term Biodistribution, and Toxicology of PEGylated Graphene in Mice ACS Nano 2011, 5, 516-522
9. Wang, K.; Ruan, J.; Song, H.; Zhang, J. L.; Wo, Y.; Guo, S. W.; Cui, D. X. Biocompatibility of Graphene Oxide Nanoscale Res. Lett. 2011, 6, 8
10. Zhang, Y. B.; Ali, S. F.; Dervishi, E.; Xu, Y.; Li, Z. R.; Casciano, D.; Biris, A. S. Cytotoxicity Effects of Graphene and Single-Wall Carbon Nanotubes in Neural Phaeochromocytoma-Derived PC12 Cells ACS Nano 2010, 4, 3181-3186
11. Varin, A.; Gordon, S. Alternative Activation of Macrophages: Immune Function and Cellular Biology Immunobiology 2009, 214, 630-641
12. Liao, K. H.; Lin, Y. S.; Macosko, C. W.; Haynes, C. L. Cytotoxicity of Graphene Oxide and Graphene in Human Erythrocytes and Skin Fibroblasts ACS Appl. Mater. Interfaces 2011, 3, 2607-2615
13. Singh, S. K.; Singh, M. K.; Nayak, M. K.; Kumari, S.; Shrivastava, S.; Gracio, J. J. A.; Dash, D. Thrombus Inducing Property of Atomically Thin Graphene Oxide Sheets ACS Nano 2011, 5, 4987-4996
14. Sasidharan, A.; Panchakarla, L. S.; Sadanandan, A. R.; Ashokan, A.; Chandran, P.; Girish, C. M.; Menon, D.; Nair, S. V.; Rao, C. N.; Koyakutty, M. Hemocompatibility and Macrophage Response of Pristine and Functionalized Graphene Small 2012, 8, 1251-1263
15. Sasidharan, A.; Panchakarla, L. S.; Chandran, P.; Menon, D.; Nair, S.; Rao, C. N. R.; Koyakutty, M. Differential Nano-Bio Interactions and Toxicity Effects of Pristine versus Functionalized Graphene Nanoscale 2011, 3, 2461-2464
16. Li, Y.; Liu, Y.; Fu, Y. J.; Wei, T. T.; Le Guyader, L.; Gao, G.; Liu, R. S.; Chang, Y. Z.; Chen, C. Y. The Triggering of Apoptosis in Macrophages by Pristine Graphene through the MAPK and TGF-Beta Signaling Pathways Biomaterials 2012, 33, 402-411
17. Chen, G. Y.; Yang, H. J.; Lu, C. H.; Chao, Y. C.; Hwang, S. M.; Chen, C. L.; Lo, K. W.; Sung, L. Y.; Luo, W. Y.; Tuan, H. Y. et al. Simultaneous Induction of Autophagy and Toll-Like Receptor Signaling Pathways by Graphene Oxide Biomaterials 2012, 33, 6559-6569
18. Cho, Y. S.; Challa, S.; Moquin, D.; Genga, R.; Ray, T. D.; Guildford, M.; Chan, F. K. Phosphorylation-Driven Assembly of the RIP1-RIP3 Complex Regulates Programmed Necrosis and Virus-Induced Inflammation Cell 2009, 137, 1112-1123
19. Han, J. H.; Zhong, C. Q.; Zhang, D. W. Programmed Necrosis: Backup to and Competitor with Apoptosis in the Immune System Nat. Immunol. 2011, 12, 1143-1149
20. Fortes, G. B.; Alves, L. S.; de Oliveira, R.; Dutra, F. F.; Rodrigues, D.; Fernandez, P. L.; Souto-Padron, T.; De Rosa, M. J.; Kelliher, M.; Golenbock, D. et al. Heme Induces Programmed Necrosis on Macrophages through Autocrine TNF and ROS Production Blood 2012, 119, 2368-2375
21. Vandenabeele, P.; Galluzzi, L.; Vanden Berghe, T.; Kroemer, G. Molecular Mechanisms of Necroptosis: An Ordered Cellular Explosion Nat. Rev. Mol. Cell Biol. 2010, 11, 700-714
22. Challa, S.; Chan, F. K. M. Going up in Flames: Necrotic Cell Injury and Inflammatory Diseases Cell. Mol. Life Sci. 2010, 67, 3241-3253
23. Poltorak, A.; He, X. L.; Smirnova, I.; Liu, M. Y.; Van Huffel, C.; Du, X.; Birdwell, D.; Alejos, E.; Silva, M.; Galanos, C. et al. Defective LPS Signaling in C3H/HeJ and C57BL/10ScCr Mice: Mutations in TLR4 Gene Science 1998, 282, 2085-2088
24. Verma, A.; Ngundi, M. M.; Meade, B. D.; De Pascalis, R.; Elkins, K. L.; Burns, D. L. Analysis of the Fc Gamma Receptor-Dependent Component of Neutralization Measured by Anthrax Toxin Neutralization Assays Clin. Vaccine Immunol. 2009, 16, 1405-1412
25. Godek, M. L.; Duchsherer, N. L.; McElwee, Q.; Grainger, D. W. Morphology and Growth of Murine Cell Lines on Model Biomaterials Biomed. Sci. Instrum. 2004, 40, 7-12
26. Nicholson, D. W.; Ali, A.; Thornberry, N. A.; Vaillancourt, J. P.; Ding, C. K.; Gallant, M.; Gareau, Y.; Griffin, P. R.; Labelle, M.; Lazebnik, Y. A. et al. Identification and Inhibition of the ICE/CED-3 Protease Necessary for Mammalian Apoptosis Nature 1995, 376, 37-43
27. Bohrer, D.; Horner, R.; do Nascimento, P. C.; Adaime, M.; Pereira, M. E.; Martins, A. F.; Hartz, S. A. Interference in the Limulus Amebocyte Lysate Assay for Endotoxin Determination in Peritoneal Dialysis Fluids and Concentrates for Hemodialysis J. Pharm. Biomed. Anal. 2001, 26, 811-818
28. Huang, K. J.; Niu, D. J.; Sun, J. Y.; Han, C. H.; Wu, Z. W.; Li, Y. L.; Xiong, X. Q. Novel Electrochemical Sensor Based on Functionalized Graphene for Simultaneous Determination of Adenine and Guanine in DNA Colloid Surf., B 2011, 82, 543-549
29. Singh, S. K.; Singh, M. K.; Kulkarni, P. P.; Sonkar, V. K.; Gracio, J. J. A.; Dash, D. Amine-Modified Graphene. Thrombo-Protective Safer Alternative to Graphene Oxide for Biomedical Applications ACS Nano 2012, 6, 2731-2740
30. Zhou, H. J.; Zhao, K.; Li, W.; Yang, N.; Liu, Y.; Chen, C. Y.; Wei, T. T. The Interactions between Pristine Graphene and Macrophages and the Production of Cytokines/Chemokines via TLR- and NF-KappaB-Related Signaling Pathways Biomaterials 2012, 33, 6933-6942
31. Li, S. T.; Wang, L. Y.; Berman, M.; Kong, Y. Y.; Dorf, M. E. Mapping a Dynamic Innate Immunity Protein Interaction Network Regulating Type I Interferon Production Immunity 2011, 35, 426-440
32. Wei, Y.; Wang, B.; Wu, J.; Yang, R.; Dunn, M. L. Bending Rigidity and Gaussian Bending Stiffness of Single-Layered Graphene Nano Lett. 2013, 13, 26-30
33. Linkermann, A.; Brasen, J. H.; De Zen, F.; Weinlich, R.; Schwendener, R. A.; Green, D. R.; Kunzendorf, U.; Krautwald, S. Dichotomy between RIP1- and RIP3-Mediated Necroptosis in Tumor Necrosis Factor-Alpha-Induced Shock Mol. Med. 2012, 18, 577-586
34. Cho, Y.; Challa, S.; Moquin, D.; Genga, R.; Ray, T. D.; Guildford, M.; Chan, F. K. M. Phosphorylation-Driven Assembly of the RIP1-RIP3 Complex Regulates Programmed Necrosis and Virus-Induced Inflammation Cell 2009, 137, 1112-1123
35. Festjens, N.; Vanden Berghe, T.; Cornelis, S.; Vandenabeele, P. RIP1, a Kinase on the Crossroads of a Cell's Decision to Live or Die Cell Death Differ. 2007, 14, 400-410
36. Aoki, K.; Saito, H.; Itzstein, C.; Ishiguro, M.; Shibata, T.; Blanque, R.; Mian, A. H.; Takahashi, M.; Suzuki, Y.; Yoshimatsu, M. et al. A TNF Receptor Loop Peptide Mimic Blocks Rank Ligand-Induced Signaling, Bone Resorption, and Bone Loss J. Clin. Invest. 2006, 116, 1525-1534
37. McComb, S.; Cheung, H. H.; Korneluk, R. G.; Wang, S.; Krishnan, L.; Sad, S. cIAP1 and cIAP2 Limit Macrophage Necroptosis by Inhibiting RIP1 and RIP3 Activation Cell Death Differ. 2012, 1791-1801
38. Vanlangenakker, N.; Bertrand, M. J. M.; Bogaert, P.; Vandenabeele, P.; Vanden Berghe, T. TNF-Induced Necroptosis in L929 Cells is Tightly Regulated by Multiple TNFR1 Complex I and II Members Cell Death Dis. 2011, 2, e230
39. Tamura, Y.; Chiba, Y.; Tanioka, T.; Shimizu, N.; Shinozaki, S.; Yamada, M.; Kaneki, K.; Mori, S.; Araki, A.; Ito, H. et al. No Donor Induces Nec-1-Inhibitable, but RIP1-Independent, Necrotic Cell Death in Pancreatic Beta-Cells FEBS Lett. 2011, 585, 3058-3064
40. Roychowdhury, S.; McMullen, M. R.; Pisano, S. G.; Liu, X. L.; Nagy, L. E. Absence of Receptor Interacting Protein Kinase 3 Prevents Ethanol-Induced Liver Injury Hepatology 2012, 57, 1773-1783
41. Azijli, K.; Yuvaraj, S.; Peppelenbosch, M. P.; Wurdinger, T.; Dekker, H.; Joore, J.; van Dijk, E.; Quax, W. J.; Peters, G. J.; de Jong, S. et al. Kinome Profiling of Non-Canonical TRAIL Signaling Reveals RIP1-Src-STAT3-Dependent Invasion in Resistant Non-Small Cell Lung Cancer Cells J. Cell Sci. 2012, 125, 4651-4661
42. Degterev, A.; Hitomi, J.; Germscheid, M.; Ch'en, I. L.; Korkina, O.; Teng, X.; Abbott, D.; Cuny, G. D.; Yuan, C.; Wagner, G. et al. Identification of RIP1 Kinase as a Specific Cellular Target of Necrostatins Nat. Chem. Biol. 2008, 4, 313-321
43. Liu, S. J.; Goldstein, R. H.; Scepansky, E. M.; Rosenblatt, M. Inhibition of Rho-Associated Kinase Signaling Prevents Breast Cancer Metastasis to Human Bone Cancer Res. 2009, 69, 8742-8751
44. Johnson-Lyles, D. N.; Peifley, K.; Lockett, S.; Neun, B. W.; Hansen, M.; Clogston, J.; Stern, S. T.; McNeil, S. E. Fullerenol Cytotoxicity in Kidney Cells Is Associated with Cytoskeleton Disruption, Autophagic Vacuole Accumulation, and Mitochondrial Dysfunction Toxicol. Appl. Pharmacol. 2010, 248, 249-258
45. Liu, S. J.; Suragani, R. N. V. S.; Wang, F. D.; Han, A. P.; Zhao, W. T.; Andrews, N. C.; Chen, J. J. The Function of Heme-Regulated eIF2 Alpha Kinase in Murine Iron Homeostasis and Macrophage Maturation J. Clin. Invest. 2007, 117, 3296-3305
46. Riento, K.; Ridley, A. J. Rocks: Multifunctional Kinases in Cell Behaviour Nat. Rev. Mol. Cell Biol. 2003, 4, 446-456
47. Uehata, M.; Ishizaki, T.; Satoh, H.; Ono, T.; Kawahara, T.; Morishita, T.; Tamakawa, H.; Yamagami, K.; Inui, J.; Maekawa, M. et al. Calcium Sensitization of Smooth Muscle Mediated by a Rho-Associated Protein Kinase in Hypertension Nature 1997, 389, 990-994
48. Liu, S. J. The Rock Signaling and Breast Cancer Metastasis Mol. Biol. Rep. 2011, 38, 1363-1366
49. Matsuzawa, A.; Saegusa, K.; Noguchi, T.; Sadamitsu, C.; Nishitoh, H.; Nagai, S.; Koyasu, S.; Matsumoto, K.; Takeda, K.; Ichijo, H. ROS-Dependent Activation of the TRAF6-ASK1-p38 Pathway Is Selectively Required for TLR4-Mediated Innate Immunity Nat. Immunol. 2005, 6, 587-592
50. Nel, A.; Xia, T.; Madler, L.; Li, N. Toxic Potential of Materials at the Nanolevel Science 2006, 311, 622-627
51. Sayes, C. M.; Gobin, A. M.; Ausman, K. D.; Mendez, J.; West, J. L.; Colvin, V. L. Nano-C60 Cytotoxicity Is Due to Lipid Peroxidation Biomaterials 2005, 26, 7587-7595
52. Xia, T.; Kovochich, M.; Brant, J.; Hotze, M.; Sempf, J.; Oberley, T.; Sioutas, C.; Yeh, J. I.; Wiesner, M. R.; Nel, A. E. Comparison of the Abilities of Ambient and Manufactured Nanoparticles to Induce Cellular Toxicity According to an Oxidative Stress Paradigm Nano Lett. 2006, 6, 1794-1807
53. Xia, T. A.; Zhao, Y.; Sager, T.; George, S.; Pokhrel, S.; Li, N.; Schoenfeld, D.; Meng, H. A.; Lin, S. J.; Wang, X. et al. Decreased Dissolution of ZnO by Iron Doping Yields Nanoparticles with Reduced Toxicity in the Rodent Lung and Zebrafish Embryos ACS Nano 2011, 5, 1223-1235
54. Jayalakshmi, K.; Sairam, M.; Singh, S. B.; Sharma, S. K.; Ilavazhagan, G.; Banerjee, P. K. Neuroprotective Effect of N-Acetyl Cysteine on Hypoxia-Induced Oxidative Stress in Primary Hippocampal Culture Brain Res. 2005, 1046, 97-104
55. Chen, L. Q.; Qu, G. B.; Sun, X.; Zhang, S. P.; Wang, L.; Sang, N. G.; Du, Y. G.; Liu, J.; Liu, S. J. Characterization of the Interaction between Cadmium and Chlorpyrifos with Integrative Techniques in Incurring Synergistic Hepatoxicity PLoS One 2013, 8, e59553
56. Colvin, V. L. The Potential Environmental Impact of Engineered Nanomaterials Nat. Biotechnol. 2003, 21, 1166-1170
57. Li, X.; Peng, Y.; Ren, J.; Qu, X. Carboxyl-Modified Single-Walled Carbon Nanotubes Selectively Induce Human Telomeric I-Motif Formation Proc. Nat. Acad. Sci. U.S.A. 2006, 103, 19658-19663
58. Rodriguez-Fernandez, L.; Valiente, R.; Gonzalez, J.; Villegas, J. C.; Fanarraga, M. L. Multiwalled Carbon Nanotubes Display Microtubule Biomimetic Properties in Vivo, Enhancing Microtubule Assembly and Stabilization ACS Nano 2012, 6, 6614-6625
59. Zhu, Y. W.; Murali, S.; Cai, W. W.; Li, X. S.; Suk, J. W.; Potts, J. R.; Ruoff, R. S. Graphene and Graphene Oxide: Synthesis, Properties, and Applications Adv. Mater. 2010, 22, 3906-3924
60. Nguyen, P.; Berry, V. Graphene Interfaced with Biological Cells: Opportunities and Challenges J. Phys. Chem. Lett. 2012, 3, 1024-1029
61. Nel, A. E.; Madler, L.; Velegol, D.; Xia, T.; Hoek, E. M. V.; Somasundaran, P.; Klaessig, F.; Castranova, V.; Thompson, M. Understanding Biophysicochemical Interactions at the Nano-Bio Interface Nat. Mater. 2009, 8, 543-557
62. Mu, Q.; Du, G.; Chen, T.; Zhang, B.; Yan, B. Suppression of Human Bone Morphogenetic Protein Signaling by Carboxylated Single-Walled Carbon Nanotubes ACS Nano 2009, 3, 1139-1144
63. Zhang, H. Y.; Xia, T.; Meng, H.; Xue, M.; George, S.; Ji, Z. X.; Wang, X.; Liu, R.; Wang, M. Y.; France, B. et al. Differential Expression of Syndecan-1 Mediates Cationic Nanoparticle Toxicity in Undifferentiated versus Differentiated Normal Human Bronchial Epithelial Cells ACS Nano 2011, 5, 2756-2769
64. Jia, X. T.; Hofmann, M.; Meunier, V.; Sumpter, B. G.; Campos-Delgado, J.; Romo-Herrera, J. M.; Son, H. B.; Hsieh, Y. P.; Reina, A.; Kong, J. et al. Controlled Formation of Sharp Zigzag and Armchair Edges in Graphitic Nanoribbons Science 2009, 323, 1701-1705
65. Qu, G. B.; Wang, X. Y.; Wang, Z.; Liu, S. J.; Jiang, G. B. Cytotoxicity of Quantum Dots and Graphene Oxide to Erythroid Cells and Macrophages Nanoscale Res. Lett. 2013, 8, 198
66. Jorda, E. G.; Verdaguer, E.; Jimenez, A.; de Arriba, S. G.; Allgaier, C.; Pallas, M.; Camins, A. Evaluation of the Neuronal Apoptotic Pathways Involved in Cytoskeletal Disruption-Induced Apoptosis Biochem. Pharmacol. 2005, 70, 470-480
67. Sandbo, N.; Dulin, N. Featured New Investigator Actin Cytoskeleton in Myofibroblast Differentiation: Ultrastructure Defining Form and Driving Function Transl. Res. 2011, 158, 181-196
68. Kristensen, B. W.; Noer, H.; Gramsbergen, J. B.; Zimmer, J.; Noraberg, J. Colchicine Induces Apoptosis in Organotypic Hippocampal Slice Cultures Brain Res. 2003, 964, 264-278
69. Schindler, B.; Segal, E. Candida albicans Metabolite Affects the Cytoskeleton and Phagocytic Activity of Murine Macrophages Med. Mycol. 2008, 46, 251-258
70. Fettucciari, K.; Quotadamo, F.; Noce, R.; Palumbo, C.; Modesti, A.; Rosati, E.; Mannucci, R.; Bartoli, A.; Marconi, P. Group B Streptococcus (Gbs) Disrupts by Calpain Activation the Actin and Microtubule Cytoskeleton of Macrophages Cell. Microbiol. 2011, 13, 859-884
71. Liu, Q.; Shi, J. B.; Sun, J. T.; Wang, T.; Zeng, L. X.; Jiang, G. B. Graphene and Graphene Oxide Sheets Supported on Silica as Versatile and High-Performance Adsorbents for Solid-Phase Extraction Angew. Chem., Int. Ed. 2011, 50, 5913-5917
72. Zhou, H. Y.; Mu, Q. X.; Gao, N. N.; Liu, A. F.; Xing, Y. H.; Gao, S. L.; Zhang, Q.; Qu, G. B.; Chen, Y. Y.; Liu, G. et al. A Nano-Combinatorial Library Strategy for the Discovery of Nanotubes with Reduced Protein-Binding, Cytotoxicity, and Immune Response Nano Lett. 2008, 8, 859-865
73. Mu, Q. X.; Su, G. M.; Li, L. W.; Gilbertson, B. O.; Yu, L. H.; Zhang, Q.; Sun, Y. P.; Yan, B. Size-Dependent Cell Uptake of Protein-Coated Graphene Oxide Nanosheets ACS Appl. Mater. Interfaces 2012, 4, 2259-2266
74. Kudin, K. N.; Ozbas, B.; Schniepp, H. C.; Prud'homme, R. K.; Aksay, I. A.; Car, R. Raman Spectra of Graphite Oxide and Functionalized Graphene Sheets Nano Lett. 2008, 8, 36-41
75. Liu, R.; Liu, J. F.; Zhou, X. X.; Sun, M. T.; Jiang, G. B. Fabrication of a Au Nanoporous Film by Self-Organization of Networked Ultrathin Nanowires and Its Application as a Surface-Enhanced Raman Scattering Substrate for Single-Molecule Detection Anal. Chem. 2011, 83, 9131-9137
76. Wang, Z.; Liu, S. J.; Ma, J.; Qu, G. B.; Wang, X. Y.; Yu, S. J.; He, J. Y.; Liu, J. F.; Xia, T.; Jiang, G. B. Silver Nanoparticles Induced RNA Polymerase-Silver Binding and RNA Transcription Inhibition in Erythroid Progenitor Cells ACS Nano 2013, 28, 4171-7186
77. Liu, W.; Zhang, S. P.; Wang, L. X.; Qu, C.; Zhang, C. W.; Hong, L.; Yuan, L.; Huang, Z. H.; Wang, Z.; Liu, S. J. et al. CdSe Quantum Dot (QD)-Induced Morphological and Functional Impairments to Liver in Mice PLoS One 2011, 6, e24406