Inhibition of the proteasome activity by graphene oxide contributes to its cytotoxicity

References

• Aberle, H., A. Bauer, J. Stappert, A. Kispert, and R. Kemler. 1997. “Beta-Catenin Is a Target for the Ubiquitin-Proteasome Pathway.” The EMBO Journal 16 (13): 3797–3804. DOI: 10.1093/emboj/16.13.3797
   PubMed Web of Science ®Google Scholar
• Adams, J. 2002. “Proteasome Inhibition: A Novel Approach to Cancer Therapy.” Trends in Molecular Medicine 8 (4 Suppl): S49–S54. DOI: 10.1016/S1471-4914(02)02315-8
   Web of Science ®Google Scholar
• 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
• Best, R. B., X. Zhu, J. Shim, P. E. M. Lopes, J. Mittal, M. Feig, and A. D. MacKerell. Jr. 2012. “Optimization of the Additive CHARMM All-Atom Protein Force Field Targeting Improved Sampling of the Backbone ϕ, ψ and Side-Chain χ1 and χ2 Dihedral Angles.” Journal of Chemical Theory and Computation 8 (9): 3257–3273. DOI: 10.1021/ct300400x
   PubMed Web of Science ®Google Scholar
• Chen, D., M. Frezza, R. Shakya, Q. C. Cui, V. Milacic, C. N. Verani, and Q. P. Dou. 2007. “Inhibition of the Proteasome Activity by Gallium(III) Complexes Contributes to Their anti Prostate Tumor Effects.” Cancer Research 67 (19): 9258–9265. DOI: 10.1158/0008-5472CAN-07-1813
   PubMed Web of Science ®Google Scholar
• Chen, S., J. Wu, Y. Lu, Y.-B. Ma, B.-H. Lee, Z. Yu, Q. Ouyang, D. J. Finley, M. W. Kirschner, and Y. Mao. 2016. “Structural Basis for Dynamic Regulation of the Human 26S Proteasome.” Proceedings of the National Academy of Sciences of the United States America 113 (46): 12991–12996. DOI: 10.1073/pnas.1614614113
   PubMed Web of Science ®Google Scholar
• Chong, Y., C. Ge, Z. Yang, J. A. Garate, Z. Gu, J. K. Weber, J. Liu, and R. Zhou. 2015. “Reduced Cytotoxicity of Graphene Nanosheets Mediated by Blood-Protein Coating.” ACS Nano 9 (6): 5713–5724. DOI: 10.1021/nn5066606
   PubMed Web of Science ®Google Scholar
• Collins, A. R. 2004. “The Comet Assay for DNA Damage and Repair: Principles, Applications, and Limitations.” Molecular Biotechnology 26 (3): 249–261. DOI: 10.1385/MB:26:3:249
   PubMed Web of Science ®Google Scholar
• Darden, T., D. York, and L. Pedersen. 1993. “Particle Mesh Ewald: An N⋅Log(N) Method for Ewald Sums in Large Systems.” The Journal of Chemical Physics 98 (12): 10089–10092. DOI: 10.1063/1.464397
   Web of Science ®Google Scholar
• Daulny, A., and W. P. Tansey. 2009. “Damage Control: DNA Repair, Transcription, and the Ubiquitin-Proteasome System.” DNA Repair 8 (4): 444–448. DOI: 10.1016/j.dnarep.2009.01.017
   PubMed Web of Science ®Google Scholar
• Denizot, F., and R. Lang. 1986. “Rapid Colorimetric Assay for Cell Growth and Survival. Modifications to the Tetrazolium Dye Procedure Giving Improved Sensitivity and Reliability.” Journal of Immunological Methods 89 (2): 271–277. DOI: 10.1016/0022-1759(86)90368-6
   PubMed Web of Science ®Google Scholar
• Ding, X., H. Liu, and Y. Fan. 2015. “Graphene-Based Materials in Regenerative Medicine.” Advanced Healthcare Materials 4 (10): 1451–1468. DOI: 10.1002/adhm.201500203
   PubMed Web of Science ®Google Scholar
• Duan, G., S. G. Kang, X. Tian, J. A. Garate, L. Zhao, C. Ge, and R. Zhou. 2015. “Protein Corona Mitigates the Cytotoxicity of Graphene Oxide by Reducing Its Physical Interaction with Cell Membrane.” Nanoscale 7 (37): 15214–15224. DOI: 10.1039/c5nr01839k
   PubMed Web of Science ®Google Scholar
• Ema, M., M. Gamo, and K. Honda. 2017. “A Review of Toxicity Studies on Graphene-Based Nanomaterials in Laboratory Animals.” Regulatory Toxicology & Pharmacology 85: 7–24. DOI: 10.1016/j.yrtph.2017.01.011
   PubMed Web of Science ®Google Scholar
• Falaschetti, C. A., T. Paunesku, J. Kurepa, D. Nanavati, S. S. Chou, M. De, M. Song, et al. 2013. “Negatively Charged Metal Oxide Nanoparticles Interact with the 20S Proteasome and Differentially Modulate Its Biologic Functional Effects.” ACS Nano 7 (9): 7759–7772. DOI: 10.1021/nn402416h
   PubMed Web of Science ®Google Scholar
• Feller, S. E., Y. Zhang, R. W. Pastor, and B. R. Brooks. 1995. “Constant Pressure Molecular Dynamics Simulation: The Langevin Piston Method.” The Journal of Chemical Physics 103 (11): 4613–4621. DOI: 10.1063/1.470648
   Web of Science ®Google Scholar
• Frankland-Searby, S., and S. R. Bhaumik. 2012. “The 26S Proteasome Complex: An Attractive Target for Cancer Therapy.” Biochimica et Biophysica Acta 1825 (1): 64–76. DOI: 10.1016/j.bbcan.2011.10.003
   PubMed Web of Science ®Google Scholar
• Gagner, J. E., M. D. Lopez, J. S. Dordick, and R. W. Siegel. 2011. “Effect of Gold Nanoparticle Morphology on Adsorbed Protein Structure and Function.” Biomaterials 32 (29): 7241–7252. DOI: 10.1016/j.biomaterials.2011.05.091
   PubMed Web of Science ®Google Scholar
• Ge, C., J. Tian, Y. Zhao, C. Chen, R. Zhou, and Z. Chai. 2015. “Towards Understanding of Nanoparticle-Protein Corona.” Archives of Toxicology 89 (4): 519–539. DOI: 10.1007/s00204-015-1458-0
   PubMed Web of Science ®Google Scholar
• Glickman, M. H., and A. Ciechanover. 2002. “The Ubiquitin-Proteasome Proteolytic Pathway: Destruction for the Sake of Construction.” Physiological Reviews 82 (2): 373–428. DOI: 10.1152/physrev.00027.2001
   PubMed Web of Science ®Google Scholar
• Go´mez-Navarro, C., J. C. Meyer, R. S. Sundaram, A. Chuvilin, S. Kurasch, M. Burghard, K. Kern, and U. Kaiser. 2010. “Atomic Structure of Reduced Graphene Oxide.” Nano Letters 10 (4): 1144–1148. DOI: 10.1021/nl9031617
   PubMed Web of Science ®Google Scholar
• Grossfield, A. 2003. WHAM: An Implementation of the Weighted Histogram Analysis Method. Rochester, NY: Grossfield Lab. http://membrane.urmc.rochester.edu/content/wham.
   Google Scholar
• Han, J. H., E. J. Lee, J. H. Lee, K. P. So, Y. H. Lee, G. N. Bae, S. B. Lee, J. H. Ji, M. H. Cho, and I. J. Yu. 2008. “Monitoring Multiwalled Carbon Nanotube Exposure in Carbon Nanotube Research Facility.” Inhalation Toxicology 20 (8): 741–749. DOI: 10.1080/08958370801942238
   PubMed Web of Science ®Google Scholar
• Heinemeyer, W., M. Fischer, T. Krimmer, U. Stachon, and D. H. Wolf. 1997. “The Active Sites of the Eukaryotic 20S Proteasome and Their Involvement in Subunit Precursor Processing.” Journal of Biological Chemistry 272 (40): 25200–25209. DOI: 10.1074/jbc.272.40.25200
   PubMed Web of Science ®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
• Huber, E. M., M. Basler, R. Schwab, W. Heinemeyer, C. J. Kirk, M. Groettrup, and M. Groll. 2012. “Immuno- and Constitutive Proteasome Crystal Structures Reveal Differences in Substrate and Inhibitor Specificity.” Cell 148 (4): 727–738. DOI: 10.1016/j.cell.2011.12.030
   PubMed Web of Science ®Google Scholar
• Huber, E. M., W. Heinemeyer, X. Li, C. S. Arendt, M. Hochstrasser, and M. Groll. 2016. “A Unified Mechanism for Proteolysis and Autocatalytic Activation in the 20S Proteasome.” Nature Communications 7: 10900. DOI: 10.1038/ncomms10900
   PubMed Web of Science ®Google Scholar
• Hummer, G., J. C. Rasaiah, and J. P. Noworyta. 2001. “Water Conduction through the Hydrophobic Channel of a Carbon Nanotube.” Nature 414 (6860): 188–190. DOI: 10.1038/35102535
   PubMed Web of Science ®Google Scholar
• Humphrey, W., A. Dalke, and K. Schulten. 1996. “VMD: Visual Molecular Dynamics.” Journal of Molecular Graphics 14 (1): 33–38. 27-38. DOI: 10.1016/0263-7855(96)00018-5
   PubMedGoogle Scholar
• Jo, S., T. Kim, V. G. Iyer, and W. Im. 2008. “CHARMM-GUI: A Web-Based Graphical User Interface for CHARMM.” Journal of Computational Chemistry 29 (11): 1859–1865. DOI: 10.1002/jcc.20945
   PubMed Web of Science ®Google Scholar
• Jorgensen, W. L., J. Chandrasekhar, J. D. Madura, R. W. Impey, and M. L. Klein. 1983. “Comparison of Simple Potential Functions for Simulating Liquid Water.” The Journal of Chemical Physics 79 (2): 926–935. DOI: 10.1063/1.445869
   Web of Science ®Google Scholar
• Karimian, A., Y. Ahmadi, and B. Yousefi. 2016. “Multiple Functions of p21 in Cell Cycle, Apoptosis and Transcriptional Regulation after DNA Damage.” DNA Repair (Amsterdam) 42: 63–71. DOI: 10.1016/j.dnarep.2016.04.008
   PubMed Web of Science ®Google Scholar
• Kisselev, A. F., and A. L. Goldberg. 2001. “Proteasome Inhibitors: From Research Tools to Drug Candidates.” Chemistry &Amp; Biology 8 (8): 739–758. DOI: 10.1016/S1074-5521(01)00056-4
   PubMed Web of Science ®Google Scholar
• Kumar, P. J., and B. Kwang-Hyun. 2016. “Comparative Study of Proteasome Inhibitory, Synergistic Antibacterial, Synergistic Anticandidal, and Antioxidant Activities of Gold Nanoparticles Biosynthesized Using Fruit Waste Materials.” International Journal of Nanomedicine 11: 4691. DOI: 10.2147/IJN.S108920
   PubMed Web of Science ®Google Scholar
• Kumar, S., J. M. Rosenberg, D. Bouzida, R. H. Swendsen, and P. A. Kollman. 1992. “The Weighted Histogram Analysis Method for Free-Energy Calculations on Biomolecules. I. The Method.” Journal of Computational Chemistry 13 (8): 1011–1021. DOI: 10.1002/jcc.540130812
   Web of Science ®Google Scholar
• Lee, D. H., and A. L. Goldberg. 1998. “Proteasome Inhibitors: Valuable New Tools for Cell Biologists.” Trends in Cell Biology 8 (10): 397–403. DOI: 10.1016/S0962-8924(98)01346-4
   PubMed Web of Science ®Google Scholar
• Li, R., X. Wang, Z. Ji, B. Sun, H. Zhang, C. H. Chang, S. Lin, et al. 2013. “Surface Charge and Cellular Processing of Covalently Functionalized Multiwall Carbon Nanotubes Determine Pulmonary Toxicity.” ACS Nano 7 (3): 2352. DOI: 10.1021/nn305567s
   PubMed Web of Science ®Google Scholar
• Li, Y., Y. Liu, Y. Fu, T. Wei, L. Le Guyader, G. Gao, R. S. Liu, Y. Z. Chang, and C. Chen. 2012. “The Triggering of Apoptosis in Macrophages by Pristine Graphene through the MAPK and TGF-Beta Signaling Pathways.” Biomaterials 33 (2): 402–411. DOI: 10.1016/j.biomaterials.2011.09.091
   PubMed Web of Science ®Google Scholar
• Lowe, J., D. Stock, B. Jap, P. Zwickl, W. Baumeister, and R. Huber. 1995. “Crystal Structure of the 20S Proteasome from the Archaeon T. acidophilum at 3.4 a Resolution.” Science 268 (5210): 533–539. DOI: 10.1126/science.7725097
   PubMed Web of Science ®Google Scholar
• Manton, C. A., B. Johnson, M. Singh, C. P. Bailey, L. Bouchier-Hayes, and J. Chandra. 2016. “Induction of Cell Death by the Novel Proteasome Inhibitor Marizomib in Glioblastoma in Vitro and in Vivo.” Scientific Reports 6 (1): 18953. DOI: 10.1038/srep18953
   PubMedGoogle Scholar
• Martyna, G. J., D. J. Tobias, and M. L. Klein. 1994. “Constant Pressure Molecular Dynamics Algorithms.” The Journal of Chemical Physics 101 (5): 4177–4189. DOI: 10.1063/1.467468
   Web of Science ®Google Scholar
• Miyamoto, S., and P. A. Kollman. 1992. “Settle: An Analytical Version of the SHAKE and RATTLE Algorithm for Rigid Water Models.” Journal of Computational Chemistry 13 (8): 952–962. DOI: 10.1002/jcc.540130805
   Web of Science ®Google Scholar
• Muratani, M., and W. P. Tansey. 2003. “How the Ubiquitin-Proteasome System Controls Transcription.” Nature Reviews. Molecular Cell Biology 4 (3): 192–201. DOI: 10.1038/nrm1049
   PubMed Web of Science ®Google Scholar
• Nosé, S. 1984. “A Unified Formulation of the Constant Temperature Molecular Dynamics Methods.” The Journal of Chemical Physics 81 (1): 511–519. DOI: 10.1063/1.447334
   Web of Science ®Google Scholar
• Orecchioni, M., R. Cabizza, A. Bianco, and L. G. Delogu. 2015. “Graphene as Cancer Theranostic Tool: Progress and Future Challenges.” Theranostics 5 (7): 710–723. DOI: 10.7150/thno.11387
   PubMed Web of Science ®Google Scholar
• Pagano, M., S. W. Tam, A. M. Theodoras, P. Beer-Romero, G. Del Sal, V. Chau, P. R. Yew, G. F. Draetta, and M. Rolfe. 1995. “Role of the Ubiquitin-Proteasome Pathway in Regulating Abundance of the Cyclin-Dependent Kinase Inhibitor p27.” Science 269 (5224): 682–685. DOI: 10.1126/science.7624798
   PubMed Web of Science ®Google Scholar
• Patra, J. K., M. S. Ali, I. G. Oh, and K. H. Baek. 2017. “Proteasome Inhibitory, Antioxidant, and Synergistic Antibacterial and Anticandidal Activity of Green Biosynthesized Magnetic Fe3O4 Nanoparticles Using the Aqueous Extract of Corn (Zea mays L.) Ear Leaves.” Artificial Cells, Nanomedicine and Biotechnology 45 (2): 349. DOI: 10.3109/21691401.2016.1153484
   PubMed Web of Science ®Google Scholar
• Perreault, F., A. F. de Faria, S. Nejati, and M. Elimelech. 2015. “Antimicrobial Properties of Graphene Oxide Nanosheets: Why Size Matters.” ACS Nano 9 (7): 7226–7236. DOI: 10.1021/acsnano.5b02067
   PubMed Web of Science ®Google Scholar
• Phillips, J. C., R. Braun, W. Wang, J. Gumbart, E. Tajkhorshid, E. Villa, C. Chipot, R. D. Skeel, L. Kalé, and K. Schulten. 2005. “Scalable Molecular Dynamics with NAMD.” Journal of Computational Chemistry 26 (16): 1781–1802. DOI: 10.1002/jcc.20289
   PubMed Web of Science ®Google Scholar
• Ryckaert, J.-P., G. Ciccotti, and H. J. C. Berendsen. 1977. “Numerical Integration of the Cartesian Equations of Motion of a System with Constraints: Molecular Dynamics of n-Alkanes.” Journal of Computational Physics 23 (3): 327–341. DOI: 10.1016/0021-9991(77)90098-5
   Web of Science ®Google Scholar
• Shang, F., and A. Taylor. 2011. “Ubiquitin-Proteasome Pathway and Cellular Responses to Oxidative Stress.” Free Radical Biology & Medicine 51 (1): 5–16. DOI: 10.1016/j.freeradbiomed.2011.03.031
   PubMed Web of Science ®Google Scholar
• Sun, X., Z. Liu, K. Welsher, J. T. Robinson, A. Goodwin, S. Zaric, and H. Dai. 2008. “Nano-Graphene Oxide for Cellular Imaging and Drug Delivery.” Nano Research 1 (3): 203–212. DOI: 10.1007/s12274-008-8021-8
   PubMed Web of Science ®Google Scholar
• Taylor, J. P., J. Hardy, and K. H. Fischbeck. 2002. “Toxic Proteins in Neurodegenerative Disease.” Science (New York, N.Y.) 296 (5575): 1991–1995. DOI: 10.1126/science.1067122
   PubMed Web of Science ®Google Scholar
• Tice, R. R., E. Agurell, D. Anderson, B. Burlinson, A. Hartmann, H. Kobayashi, Y. Miyamae, E. Rojas, J. C. Ryu, and Y. F. Sasaki. 2000. “Single Cell Gel/Comet Assay: Guidelines for in Vitro and in Vivo Genetic Toxicology Testing.” Environmental and Molecular Mutagenesis 35 (3): 206–221. DOI: 10.1002/(SICI)1098-2280(2000)35:3<206::AID-EM8>3.0.CO;2-J
   PubMed Web of Science ®Google Scholar
• Tribello, G. A., M. Bonomi, D. Branduardi, C. Camilloni, and G. Bussi. 2014. “PLUMED 2: New Feathers for an Old Bird.” Computer Physics Communications 185 (2): 604–613. DOI: 10.1016/j.cpc.2013.09.018
   Web of Science ®Google Scholar
• Tu, Y., M. Lv, P. Xiu, T. Huynh, M. Zhang, M. Castelli, Z. Liu, et al. 2013. “Destructive Extraction of Phospholipids from Escherichia Coli Membranes by Graphene Nanosheets.” Nature Nanotechnology 8: 594–601. DOI: 10.1038/nnano.2013.125
   PubMed Web of Science ®Google Scholar
• Wang, J., U. B. Jensen, G. V. Jensen, S. Shipovskov, V. S. Balakrishnan, D. Otzen, J. S. Pedersen, F. Besenbacher, and D. S. Sutherland. 2011. “Soft Interactions at Nanoparticles Alter Protein Function and Conformation in a Size Dependent Manner.” Nano Letters 11 (11): 4985–4991. DOI: 10.1021/nl202940k
   PubMed Web of Science ®Google Scholar
• Wei, Y., F. Zhou, D. Zhang, Q. Chen, and D. Xing. 2016. “A Graphene Oxide Based Smart Drug Delivery System for Tumor Mitochondria-Targeting Photodynamic Therapy.” Nanoscale 8 (6): 3530–3538. DOI: 10.1039/c5nr07785k
   PubMed Web of Science ®Google Scholar
• Yang, K., L. Feng, and Z. Liu. 2016. “Stimuli Responsive Drug Delivery Systems Based on Nano-Graphene for Cancer Therapy.” Advanced Drug Delivery Reviews 105 (Pt B): 228–241. DOI: 10.1016/j.addr.2016.05.015
   PubMed Web of Science ®Google Scholar
• Yoo, J. M., J. H. Kang, and B. H. Hong. 2015. “Graphene-Based Nanomaterials for Versatile Imaging Studies.” Chemical Society Reviews 44 (14): 4835–4852. DOI: 10.1039/c5cs00072f
   PubMed Web of Science ®Google Scholar
• Zhou, H., B. Zhang, J. Zheng, M. Yu, T. Zhou, K. Zhao, Y. Jia, X. Gao, C. Chen, and T. Wei. 2014. “The Inhibition of Migration and Invasion of Cancer Cells by Graphene via the Impairment of Mitochondrial Respiration.” Biomaterials 35 (5): 1597–1607. DOI: 10.1016/j.biomaterials.2013.11.020
   PubMed Web of Science ®Google Scholar
• Zhou, H., K. Zhao, W. Li, N. Yang, Y. Liu, C. Chen, and T. Wei. 2012. “The Interactions between Pristine Graphene and Macrophages and the Production of Cytokines/Chemokines via TLR- and NF-kappaB-Related Signaling Pathways.” Biomaterials 33 (29): 6933–6942. DOI: 10.1016/j.biomaterials.2012.06.064
   PubMed Web of Science ®Google Scholar
• Zuo, G., X. Zhou, Q. Huang, H. Fang, and R. Zhou. 2011. “Adsorption of Villin Headpiece onto Graphene, Carbon Nanotube, and C60: Effect of Contacting Surface Curvatures on Binding Affinity.” The Journal of Physical Chemistry C 115 (47): 23323–23328. DOI: 10.1021/jp208967t
   Web of Science ®Google Scholar