Investigating oxidation state-induced toxicity of PEGylated graphene oxide in ocular tissue using gene expression profiles

References

• Akhavan, O., and E. Ghaderi. 2010. “Toxicity of Graphene and Graphene Oxide Nanowalls Against Bacteria.” ACS Nano 4 (10): 5731–5736. doi:10.1021/nn101390x.
   PubMed Web of Science ®Google Scholar
• Bajak, E., M. Fabbri, J. Ponti, S. Gioria, I. Ojea-Jiménez, A. Collotta, V. Mariani, D. Gilliland, F. Rossi, and L. Gribaldo. 2015. “Changes in Caco-2 Cells Transcriptome Profiles Upon Exposure to Gold Nanoparticles.” Toxicology Letters 233 (2): 187–199.doi:10.1016/j.toxlet.2014.12.008.
   PubMed Web of Science ®Google Scholar
• Bhattacharjee, S., L. H. J., de Haan, N. M., Evers, X., Jiang, A. T. M., Marcelis, H., Zuilhof, I. M. C. M., Rietjens, and G. M. Alink. 2010. “Role of Surface Charge and Oxidative Stress in Cytotoxicity of Organic Monolayer-Coated Silicon Nanoparticles Towards Macrophage NR8383 Cells.” Particle and Fibre Toxicology 7: 25. doi:10.1186/1743-8977-7-25.
   PubMed Web of Science ®Google Scholar
• Chang, Y., S.-T. Yang, J.-H. Liu, E. Dong, Y. Wang, A. Cao, Y. Liu, and H. Wang. 2011. “In Vitro Toxicity Evaluation of Graphene Oxide on A549 Cells.” Toxicology Letters 200 (3): 201–210. doi:10.1016/j.toxlet.2010.11.016.
   PubMed Web of Science ®Google Scholar
• Chatterjee, N., H. J. Eom, and J. Choi. 2014. “A systems toxicology approach to the surface functionality control of graphene-cell interactions.” Biomaterials 35 (4): 1109–1127. doi:10.1016/j.biomaterials.2013.09.108.
   PubMed Web of Science ®Google Scholar
• Chen, G.-Y., C.-L. Chen, H.-Y. Tuan, P.-X. Yuan, K.-C. Li, H.-J. Yang, and Y.-C. Hu. 2014. “Graphene Oxide Triggers Toll-Like Receptors/Autophagy Responses In Vitro and Inhibits Tumor Growth In Vivo.” Advanced Healthcare Materials 3 (9): 1486–1495.doi:10.1002/adhm.201300591.
   PubMed Web of Science ®Google Scholar
• Chen, G.-Y., H.-J. Yang, C.-H. Lu, Y.-C. Chao, S.-M. Hwang, C.-L. Chen, K.-W. Lo, L.-Y. Sung, W.-Y. Luo, H.-Y. Tuan, and Y.-C. Hu. 2012. “Simultaneous Induction of Autophagy and Toll-Like Receptor Signaling Pathways by Graphene Oxide.” Biomaterials 33 (27): 6559–6569.doi:10.1016/j.biomaterials.2012.05.064.
   PubMed Web of Science ®Google Scholar
• Corsi, F., C. De Palma, M. Colombo, R. Allevi, M. Nebuloni, S. Ronchi, G. Rizzi, A. Tosoni, E. Trabucchi, E. Clementi, and D. Prosperi. 2009. “Towards Ideal Magnetofluorescent Nanoparticles for Bimodal Detection of Breast-Cancer Cells.” Small 5 (22): 2555–2564.doi:10.1002/smll.200900881.
   PubMed Web of Science ®Google Scholar
• Das, S., S. Singh, V. Singh, D. Joung, J. M. Dowding, D. Reid, J. Anderson, L. Zhai, S. I. Khondaker, W. T. Self, and S. Seal. 2013. “Oxygenated Functional Group Density on Graphene Oxide: its Effect on Cell Toxicity.” Particle & Particle Systems Characterization 30 (2): 148–157.doi:10.1002/ppsc.201200066.
   Web of Science ®Google Scholar
• Duan, G., Y. Zhang, B. Luan, J. K. Weber, R. W. Zhou, Z. Yang, L. Zhao, J. Xu, J. Luo, and R. Zhou. 2017. “Graphene-Induced Pore Formation on Cell Membranes.” Science Report 7 :42767.doi:10.1038/srep42767.
   PubMed Web of Science ®Google Scholar
• Duch, M. C., G. R. S. Budinger, Y. T. Liang, S. Soberanes, D. Urich, S. E. Chiarella, L. A. Campochiaro, A. Gonzalez, N. S. Chandel, M. C. Hersam, and G. M. Mutlu. 2011. “Minimizing Oxidation and Stable Nanoscale Dispersion Improves the Biocompatibility of Graphene in the Lung.” Nano Letters 11 (12): 5201–5207.doi:10.1021/nl202515a.
   PubMed Web of Science ®Google Scholar
• Geys, J., R. De Vos, B. Nemery, and P. H. Hoet. 2009. “In Vitro Translocation of Quantum Dots and Influence of Oxidative Stress.” American Journal of Physiology-Lung Cellular and Molecular Physiology 297 (5): L903–L911.doi:10.1152/ajplung.00029.2009.
   PubMed Web of Science ®Google Scholar
• Gu, J., M. Wu, R. Guo, K. Yan, J. Lei, N. Gao, and M. Yang. 2016.doi:10.1038/nature19359. 537 (7622): 639–643.
   Google Scholar
• Hu, W., C. Peng, M. Lv, X. Li, Y. Zhang, N. Chen, C. Fan, and Q. Huang. 2011. “Protein Corona-Mediated Mitigation of Cytotoxicity of Graphene Oxide.” ACS Nano 5 (5): 3693–3700. doi:10.1021/nn200021j.
   PubMed Web of Science ®Google Scholar
• Huang, J.-F., J. Zhong, G.-P. Chen, Z.-T. Lin, Y. Deng, Y.-L. Liu, P.-Y. Cao, B. Wang, Y. Wei, T. Wu, J. Yuan, and G.-B. Jiang. 2016. “A Hydrogel-Based Hybrid Theranostic Contact Lens for Fungal Keratitis.” ACS Nano 10 (7): 6464–6473.doi:10.1021/acsnano.6b00601.
   PubMed Web of Science ®Google Scholar
• Huang, X., X. Qi, F. Boey, and H. Zhang. 2012a. “Graphene-Based Composites.” Chemical Society Reviews 41 (2): 666–686.doi:10.1039/c1cs15078b.
   PubMed Web of Science ®Google Scholar
• Huang, Y., J. Liang, and Y. Chen. 2012b. “An Overview of the Applications of Graphene-Based Materials in Supercapacitors.” Small 8 (12): 1805–1834.doi:10.1002/smll.201102635.
   PubMed Web of Science ®Google Scholar
• Hummers, W. S., and R. E. Offeman. 1958. “Preparation of Graphitic Oxide.” Journal of the American Chemical Society 80 (6): 1339–1339.doi:10.1021/ja01539a017.
   Web of Science ®Google Scholar
• Koopman, W. J. H., L. G. J. Nijtmans, C. E. J. Dieteren, P. Roestenberg, F. Valsecchi, J. A. M. Smeitink, and P. H. G. M. Willems. 2010. “Mammalian Mitochondrial Complex I: Biogenesis, Regulation, and Reactive Oxygen Species Generation.” Antioxidants and Redox Signaling 12 (12): 1431–1470.doi:10.1089/ars.2009.2743.
   PubMed Web of Science ®Google Scholar
• Kostarelos, K., and K. S. Novoselov. 2014. “Materials science. Exploring the Interface of Graphene and Biology.” Science 344 (6181): 261–263.doi:10.1126/science.1246736.
   PubMed Web of Science ®Google Scholar
• Lee, S., I. Jo, S. Kang, B. Jang, J. Moon, J. B. Park, S. Lee, S. Rho, Y. Kim, and B. H. Hong. 2017. “Smart Contact Lenses with Graphene Coating for Electromagnetic Interference Shielding and Dehydration Protection.” ACS Nano 11 (6): 5318–5324.doi:10.1021/acsnano.7b00370.
   PubMed Web of Science ®Google Scholar
• Li, L.-D., H.-F. Sun, X.-X. Liu, S.-P. Gao, H.-L. Jiang, X. Hu, and W. Jin. 2015. “Down-Regulation of NDUFB9 Promotes Breast Cancer Cell Proliferation, Metastasis by Mediating Mitochondrial Metabolism.” PloS one 10 (12): e0144441. doi:10.1371/journal.pone.0144441.
   PubMed Web of Science ®Google Scholar
• Lin, M., R. Zou, H. Shi, S. Yu, X. Li, R. Guo, L. Yan, G. Li, Y. Liu, and L. Dai. 2015. “Ocular Biocompatibility Evaluation of Hydroxyl-Functionalized Graphene.” Materials Science and Engineering C, Materials for Biological Applications 50:300–308. doi:10.1016/j.msec.2015.01.086.
   PubMed Web of Science ®Google Scholar
• Liu, X., and K. L. Chen. 2015. “Interactions of Graphene Oxide with Model Cell Membranes: Probing Nanoparticle Attachment and Lipid Bilayer Disruption.” Langmuir 31 (44): 12076–12086. doi:10.1021/acs.langmuir.5b02414.
   PubMed Web of Science ®Google Scholar
• Liu, Z., J. T. Robinson, X. Sun, and H. Dai. 2008. “PEGylated Nanographene Oxide for Delivery of Water-Insoluble Cancer Drugs.” Journal of the American Chemical Society 130 (33): 10876–10877.doi:10.1021/ja803688x
   PubMed Web of Science ®Google Scholar
• Mitsunaga, S., K. Hosomichi, Y. Okudaira, H. Nakaoka, Y. Suzuki, M. Kuwana, S. Sato, Y. Kaneko, Y. Homma, A. Oka, T. Shiina, and I. Inoue. 2015. “Aggregation of Rare/Low-Frequency Variants of the Mitochondria Respiratory Chain-Related Proteins in Rheumatoid Arthritis Patients.” Journal of Human Genetics 60 (8): 449–454.doi:10.1038/jhg.2015.50.
   PubMed Web of Science ®Google Scholar
• Nafee, N., M. Schneider, U. F. Schaefer, and C. M. Lehr. 2009. “Relevance of the Colloidal Stability of Chitosan/PLGA Nanoparticles on their Cytotoxicity Profile.” International Journal of Pharmaceutics 381 (2):130–139. doi:10.1016/j.ijpharm.2009.04.049.
   PubMed Web of Science ®Google Scholar
• Novoselov, K. S., A. K. Geim, S. V. Morozov, D. Jiang, Y. Zhang, S. V. Dubonos, I. V. Grigorieva, and A. A. Firsov. 2004. “Electric Field Effect in Atomically Thin Carbon Films.” Science 306 (5696): 666–669. doi:10.1126/science.1102896.
   PubMed Web of Science ®Google Scholar
• Oskuee, R. K., A. Dehshahri, W. T. Shier, and M. Ramezani. 2009. “Alkylcarboxylate Grafting to Polyethylenimine: a Simple Approach to Producing a DNA Nanocarrier with Low Toxicity.” The Journal of Gene Medicine 11 (10): 921–932. doi:10.1002/jgm.1374.
   PubMed Web of Science ®Google Scholar
• Purnama, A., H. Hermawan, S. Champetier, D. Mantovani, and J. Couet. 2013. “Gene Expression Profile of Mouse Fibroblasts Exposed to a Biodegradable Iron Alloy for Stents.” Acta Biomaterialia 9 (10): 8746–8753.doi:10.1016/j.actbio.2013.02.033.
   PubMed Web of Science ®Google Scholar
• Rivera Gil, P., G. Oberdörster, A. Elder, V. Puntes, and W. J. Parak. 2010. “Correlating Physico-Chemical with Toxicological Properties of Nanoparticles: the Present and the Future.” ACS Nano 4 (10): 5527–5531.doi:10.1021/nn1025687.
   PubMed Web of Science ®Google Scholar
• Ruizendaal, L., S. Bhattacharjee, K. Pournazari, M. Rosso-Vasic, L. H. J. de Haan, G. M. Alink, A. T. M. Marcelis, and H. Zuilhof. 2009. “Synthesis and Cytotoxicity of Silicon Nanoparticles with Covalently Attached Organic Monolayers.” Nanotoxicology 3 (4): 339–347.doi:10.3109/17435390903288896.
   Web of Science ®Google Scholar
• Sambrock, J. 2001. Molecular cloning: a laboratory manual. 3rd ed. New York: Cold Spring Harbor Laboratory Press.
   Google Scholar
• Sayin, B., S. Somavarapu, X. W. Li, M. Thanou, D. Sesardic, H. O. Alpar, and S. Senel. 2008. “Mono-N-Carboxymethyl Chitosan (MCC) and N-Trimethyl Chitosan (TMC) Nanoparticles for Non-Invasive Vaccine Delivery.” International Journal of Pharmaceutics 363 (1–2): 139–148.doi:10.1016/j.ijpharm.2008.06.029.
   PubMed Web of Science ®Google Scholar
• Shen, M., S. H. Wang, X. Shi, X. Chen, Q. Huang, E. J. Petersen, R. A. Pinto, J. R. Baker, and W. J. Weber. 2009. “Polyethyleneimine-Mediated Functionalization of Multiwalled Carbon Nanotubes: Synthesis, Characterization, and In Vitro Toxicity Assay.” The Journal of Physical Chemistry C 113 (8): 3150–3156.doi:10.1021/jp809323e.
   Web of Science ®Google Scholar
• Tarazona, S., F. Garcia-Alcalde, J. Dopazo, A. Ferrer, and A. Conesa. 2011. “Differential Expression in RNA-Seq: a Matter of Depth.” Genome Research 21 (12): 2213–2223.doi:10.1101/gr.124321.111.
   PubMed Web of Science ®Google Scholar
• Tonelli, F. M. P., V. A. M. Goulart, K. N. Gomes, M. S. Ladeira, A. K. Santos, E. Lorençon, L. O. Ladeira, and R. R. Resende. 2015. “Graphene-Based Nanomaterials: Biological and Medical Applications and Toxicity.” Nanomedicine (Lond) 10 (15): 2423–2450.doi:10.2217/nnm.15.65.
   PubMed Web of Science ®Google Scholar
• Tu, Y., M. Lv, P. Xiu, T. Huynh, M. Zhang, M. Castelli, Z. Liu, Q. Huang, C. Fan, H. Fang, and R. Zhou. 2013. “Destructive Extraction of Phospholipids from Escherichia coli Membranes by Graphene Nanosheets.” Nature Nanotechnology 8 (8): 594–601.doi:10.1038/nnano.2013.125.
   PubMed Web of Science ®Google Scholar
• Wan, B., Z.-X. Wang, Q.-Y. Lv, P.-X. Dong, L.-X. Zhao, Y. Yang, and L.-H. Guo. 2013. “Single-Walled Carbon Nanotubes and Graphene Oxides Induce Autophagosome Accumulation and Lysosome Impairment in Primarily Cultured Murine Peritoneal Macrophages.” Toxicology Letters 221 (2): 118–127.doi:10.1016/j.toxlet.2013.06.208.
   PubMed Web of Science ®Google Scholar
• Wang, A., K. Pu, B. Dong, Y. Liu, L. Zhang, Z. Zhang, W. Duan, and Y. Zhu. 2013. “Role of Surface Charge and Oxidative Stress in Cytotoxicity and Genotoxicity of Graphene Oxide Towards Human Lung Fibroblast Cells.” Journal of Applied Toxicology 33 (10): 1156–1164.doi:10.1002/jat.2877.
   PubMed Web of Science ®Google Scholar
• Wibroe, P. P., S. V. Petersen, N. Bovet, B. W. Laursen, and S. M. Moghimi. 2016. “Soluble and Immobilized Graphene Oxide Activates Complement System Differently Dependent on Surface Oxidation State.” Biomaterials 78 :20–26. doi:10.1016/j.biomaterials.2015.11.028.
   PubMed Web of Science ®Google Scholar
• Withers, F., T. H. Bointon, M. F. Craciun, and S. Russo. 2013. “All-Graphene Photodetectors.” ACS Nano 7 (6): 5052–5057.doi:10.1021/nn4005704.
   PubMed Web of Science ®Google Scholar
• Wu, M., J., Gu, R. Guo, Y. Huang, and M. Yang. 2016a. “Structure of Mammalian Respiratory Supercomplex I1III2IV1.” Cell 167 :1598–1609.doi:10.1016/j.cell.2016.11.012.
   PubMed Web of Science ®Google Scholar
• Wu, W., L. Yan, Q. Wu, Y. Li, Q. Li, S. Chen, Y. Yang, Z. Gu, H. Xu, and Z. Q. Yin. 2016b. “Evaluation of the Toxicity of Graphene Oxide Exposure to the Eye.” Nanotoxicology 10 (9): 1329–1340.doi:10.1080/17435390.2016.1210692.
   PubMed Web of Science ®Google Scholar
• Wu, W., Y. Zeng, Z. Li, Q. Li, H. Xu, and Z. Q. Yin. 2016c. “Features Specific to Retinal Pigment Epithelium Cells Derived from Three-Dimensional Human Embryonic Stem Cell Cultures - a New Donor for Cell Therapy.” Oncotarget 7 (16): 22819–22833.doi:10.18632/oncotarget.8185.
   PubMedGoogle Scholar
• Xu, F., Y. Yuan, X. Shan, C. Liu, X. Tao, Y. Sheng, and H. Zhou. 2009. “Long-Circulation of Hemoglobin-Loaded Polymeric Nanoparticles as Oxygen Carriers with Modulated Surface Charges.” International Journal of Pharmaceutics 377 (1–2): 199–206.doi:10.1016/j.ijpharm.2009.05.015.
   PubMed Web of Science ®Google Scholar
• Yan, L., Y.-N. Chang, L. Zhao, Z. Gu, X. Liu, G. Tian, L. Zhou, W. Ren, S. Jin, W. Yin, H. Chang, and Y. Zhao. 2013a. “The Use of Polyethylenimine-Modified Graphene Oxide as a Nanocarrier for Transferring Hydrophobic Nanocrystals into Water to Produce Water-Dispersible Hybrids for use in Drug Delivery.” Carbon 57 :120–129.doi:10.1016/j.carbon.2013.01.042.
   Web of Science ®Google Scholar
• Yan, L., GXing Li, S. Zhang, F. Sun, XJie Huang, Q. Zhang, LMing Dai, F. Lu, and Y. Liu. 2013b. “Cytotoxicity and Genotoxicity of Multi-Walled Carbon Nanotubes with Human Ocular Cells.” Chinese Science Bulletin 58 (19): 2347–2352.doi:10.1007/s11434-013-5800-8.
   Google Scholar
• Yan, L., Y. Wang, X. Xu, C. Zeng, J. Hou, M. Lin, J. Xu, F. Sun, X. Huang, L. Dai, F. Lu, and Y. Liu. 2012. “Can graphene Oxide Cause Damage to Eyesight?” Chemical Research in Toxicology 25 (6): 1265–1270.doi:10.1021/tx300129f.
   PubMed Web of Science ®Google Scholar
• Yang, T., W. Wang, H. Zhang, X. Li, J. Shi, Y. He, Q-s. Zheng, Z. Li, and H. Zhu. 2015. “Tactile Sensing System Based on Arrays of Graphene Woven Microfabrics: Electromechanical Behavior and Electronic Skin Application.” ACS Nano 9 (11): 10867–10875.doi:10.1021/acsnano.5b03851.
   PubMed Web of Science ®Google Scholar
• Zhang, P., R. Zhang, X. Fang, T. Song, X. Cai, H. Liu, and S. Du. 2016. “Toxic Effects of Graphene on the Growth and Nutritional Levels of Wheat (Triticum aestivum L.): Short- and Long-Term Exposure Studies.” Journal of Hazardous Materials 317 :543–551.doi:10.1016/j.jhazmat.2016.06.019.
   PubMed Web of Science ®Google Scholar
• Zhang, Q., Z. Wu, N. Li, Y. Pu, B. Wang, T. Zhang, and J. Tao. 2017. “Advanced Review of Graphene-Based Nanomaterials in Drug Delivery Systems: Synthesis, Modification, Toxicity and Application.” Materials Science and Engineering C: Materials for Biological Applications 77 :1363–1375.doi:10.1016/j.msec.2017.03.196.
   PubMed Web of Science ®Google Scholar
• Zhang, W., C. Wang, Z. Li, Z. Lu, Y. Li, J.-J. Yin, Y.-T. Zhou, X. Gao, Y. Fang, G. Nie, and Y. Zhao. 2012. “Unraveling Stress-Induced Toxicity Properties of Graphene Oxide and the Underlying Mechanism.” Advanced materials (Deerfield Beach, Fla.) 24 (39): 5391–5397.doi:10.1002/adma.201202678.
   PubMed Web of Science ®Google Scholar
• Zhang, W., L. Yan, M. Li, R. Zhao, X. Yang, T. Ji, Z. Gu, J.-J. Yin, X. Gao, and G. Nie. 2015. “Deciphering the Underlying Mechanisms of Oxidation-State Dependent Cytotoxicity of Graphene Oxide on Mammalian Cells.” Toxicology Letters 237 (2): 61–71.doi:10.1016/j.toxlet.2015.05.021.
   PubMed Web of Science ®Google Scholar