Proteomic profiling of RAW264.7 macrophage cells exposed to graphene oxide: insights into acute cellular responses

References

• Aksentijevich, I., S. L. Masters, P. J. Ferguson, P. Dancey, J. Frenkel, A. van Royen-Kerkhoff, R. Laxer., et al. 2009. “An Autoinflammatory Disease with Deficiency of the Interleukin-1-Receptor Antagonist.” The New England Journal of Medicine 360 (23): 2426–2437. doi:10.1056/NEJMoa0807865
   PubMed Web of Science ®Google Scholar
• Anchisi, L., S. Dessi, A. Pani, and A. Mandas. 2013. “Cholesterol Homeostasis: A Key to Prevent or Slow down Neurodegeneration.” Frontiers in Physiology 3: 486–517.
   PubMed Web of Science ®Google Scholar
• Andreyev, A. Y., Y. E. Kushnareva, and A. A. Starkov. 2005. “Mitochondrial Metabolism of Reactive Oxygen Species.” Biochemistry Biokhimiia 70 (2): 200–214. doi:10.1007/s10541-005-0102-7
   PubMed Web of Science ®Google Scholar
• Bitounis, D., H. Ali-Boucetta, B. H. Hong, D. H. Min, and K. Kostarelos. 2013. “Prospects and Challenges of Graphene in Biomedical Applications.” Advanced Materials (Deerfield Beach, Fla.) 25 (16): 2258–2268. doi:10.1002/adma.201203700
   PubMed Web of Science ®Google Scholar
• Bonaldi, T., T. Straub, J. Cox, C. Kumar, P. B. Becker, and M. Mann. 2008. “Combined Use of RNAi and Quantitative Proteomics to Study Gene Function in Drosophila.” Molecular Cell 31 (5): 762–772. doi:10.1016/j.molcel.2008.07.018
   PubMed Web of Science ®Google Scholar
• Bryan, A. M., A. M. Farnoud, V. Mor, and M. Del Poeta. 2014. “Macrophage Cholesterol Depletion and Its Effect on the Phagocytosis of Cryptococcus neoformans.” Journal of Visualized Experiments (94): 1–19. doi:10.3791/52432
   Web of Science ®Google Scholar
• Carmona-Saez, P., M. Chagoyen, F. Tirado, J. M. Carazo, and A. Pascual-Montano. 2007. “GENECODIS: A Web-Based Tool for Finding Significant Concurrent Annotations in Gene Lists.” Genome Biology 8 (1): R3. doi:10.1186/gb-2007-8-1-r3
   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
• Chellat, F., Y. Merhi, A. Moreau, and L. Yahia. 2005. “Therapeutic Potential of Nanoparticulate Systems for Macrophage Targeting.” Biomaterials 26 (35): 7260–7275. doi:10.1016/j.biomaterials.2005.05.044
   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, et al. 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
• Chen, X., S. Wei, Y. Ji, X. Guo, and F. Yang. 2015. “Quantitative Proteomics Using SILAC: Principles, Applications, and Developments.” Proteomics 15 (18): 3175–3192. doi:10.1002/pmic.201500108
   PubMed Web of Science ®Google Scholar
• Compton, O. C., and S. T. Nguyen. 2010. “Graphene Oxide, Highly Reduced Graphene Oxide, and Graphene: versatile Building Blocks for Carbon-Based Materials.” Small (Weinheim an Der Bergstrasse, Germany) 6 (6): 711–723. doi:10.1002/smll.200901934
   PubMed Web of Science ®Google Scholar
• Dimiev, A., D. V. Kosynkin, L. B. Alemany, P. Chaguine, and J. M. Tour. 2012. “Pristine Graphite Oxide.” Journal of the American Chemical Society 134 (5): 2815–2822. doi:10.1021/ja211531y
   PubMed Web of Science ®Google Scholar
• Du, Y., T. Duan, Y. Feng, Q. Liu, M. Lin, J. Cui, and R. F. Wang. 2018. “LRRC25 Inhibits Type I IFN Signaling by Targeting ISG15-Associated RIG-I for Autophagic Degradation.” The Embo Journal 37 (3): 351–366. doi:10.15252/embj.201796781
   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, et al. 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
• Franceschini, A., D. Szklarczyk, S. Frankild, M. Kuhn, M. Simonovic, A. Roth, et al. 2013. “STRING v9.1: Protein-Protein Interaction Networks, with Increased Coverage and Integration.” Nucleic Acids Res 41: 808–815.
   PubMed Web of Science ®Google Scholar
• Friedmann Angeli, J. P., M. Schneider, B. Proneth, Y. Y. Tyurina, V. A. Tyurin, V. J. Hammond, N. Herbach, et al. 2012. “Inactivation of the Ferroptosis Regulator Gpx4 Triggers Acute Renal Failure in Mice.” Nature Cell Biology 16 (12): 1180–1191. doi:10.1038/ncb3064
   Web of Science ®Google Scholar
• Garg, B., T. Bisht, and Y. C. Ling. 2015. “Graphene-Based Nanomaterials as Efficient Peroxidase Mimetic Catalysts for Biosensing Applications: An Overview.” Molecules (Basel, Switzerland) 20 (8): 14155–14190. doi:10.3390/molecules200814155
   PubMed Web of Science ®Google Scholar
• Gesquiere, L., N. Loreau, A. Minnich, J. Davignon, and D. Blache. 1999. “Oxidative Stress Leads to Cholesterol Accumulation in Vascular Smooth Muscle Cells.” Free Radical Biology and Medicine 27 (1–2): 134–145. doi:10.1016/S0891-5849(99)00055-6
   PubMed Web of Science ®Google Scholar
• Guo, X., and N. Mei. 2014. “Assessment of the Toxic Potential of Graphene Family Nanomaterials.” Journal of Food and Drug Analysis 22 (1): 105–115. doi:10.1016/j.jfda.2014.01.009
   PubMed Web of Science ®Google Scholar
• Hood, L., J. R. Heath, M. E. Phelps, and B. Lin. 2003. “Systems Biology and New Technologies Enable Predictive and Preventative Medicine.” Science 306 (5696): 640–643. doi:10.1126/science.1104635
   Web of Science ®Google Scholar
• Keshav, S., P. Chung, G. Milon, and S. Gordon. 1991. “Lysozyme Is an Inducible Marker of Macrophage Activation in Murine Tissues as Demonstrated by in Situ Hybridization.” The Journal of Experimental Medicine 174 (5): 1049–1058. doi:10.1084/jem.174.5.1049
   PubMed Web of Science ®Google Scholar
• Kiffin, R., U. Bandyopadhyay, and A. M. Cuervo. 2006. “Oxidative Stress and Autophagy.” Antioxidants & Redox Signaling 8 (1–2): 152–162. doi:10.1089/ars.2006.8.152
   PubMed Web of Science ®Google Scholar
• Krishna, K. V., C. Menard-Moyon, S. Verma, and A. Bianco. 2013. “Graphene-Based Nanomaterials for Nanobiotech-nology and Biomedical Applications.” Nanomedicine (London, England) 8 (10): 1669–1688. doi:10.2217/nnm.13.140
   PubMed Web of Science ®Google Scholar
• Lacotte, S., A. García, M. Décossas, W. T. Al-Jamal, S. P. Li, K. Kostarelos, S. Muller, M. Prato, H. Dumortier, and A. Bianco. 2008. “Interfacing Functionalized Carbon Nanohorns with Primary Phagocytic Cells.” Advanced Materials 20 (12): 2421–2426. doi:10.1002/adma.200702753
   Web of Science ®Google Scholar
• Lam, G. Y., J. Huang, and J. H. Brumell. 2010. “The Many Roles of NOX2 NADPH Oxidase-Derived ROS in Immunity.” Seminars in Immunopathology 32 (4): 415–430.
   PubMed Web of Science ®Google Scholar
• Larsen, K. B., T. Lamark, A. Overvatn, I. Harneshaug, T. Johansen, and G. Bjorkoy. 2010. “A Reporter Cell System to Monitor Autophagy Based on p62/SQSTM1.” Autophagy 6 (6): 784–793.
   PubMed Web of Science ®Google Scholar
• Li, D., M. B. Muller, S. Gilje, R. B. Kaner, and G. G. Wallace. 2008. “Processable Aqueous Dispersions of Graphene Nanosheets.” Nature Nanotechnology 3 (2): 101–105.
   PubMed Web of Science ®Google Scholar
• Li, H., Y. Li, J. Jiao, and H. M. Hu. 2011. “Alpha-Alumina Nanoparticles Induce Efficient Autophagy-Dependent Cross-Presentation and Potent Antitumour Response.” Nature Nanotechnology 6 (10): 645–650.
   PubMed Web of Science ®Google Scholar
• Li, L.,. J. Tan, Y. Miao, P. Lei, and Q. Zhang. 2015. “ROS and Autophagy: Interactions and Molecular Regulatory Mechanisms.” Cellular and Molecular Neurobiology 35 (5): 615–621.
   PubMed Web of Science ®Google Scholar
• Li, M., X. Fang, D. J. Baker, L. J. Guo, X. Gao, Z. Wei, S. H. Han, J. M. van Deursen, and P. Zhang. 2010. “The ATM-p53 Pathway Suppresses Aneuploidy-Induced Tumorigenesis.” Proceedings of the National Academy of Sciences of the United States of America 107 (32): 14188–14193.
   PubMed Web of Science ®Google Scholar
• Linares, J., M. C. Matesanz, M. Vila, M. J. Feito, G. Gonçalves, M. Vallet-Regí, P. A. A. P. Marques, and M. T. Portolés. 2014. “Endocytic Mechanisms of Graphene Oxide Nanosheets in Osteoblasts, Hepatocytes and Macrophages.” ACS Applied Materials & Interfaces 6 (16): 13697–13706.
   PubMed Web of Science ®Google Scholar
• Ma, J., R. Liu, X. Wang, Q. Liu, Y. Chen, R. P. Valle, Y. Y. Zuo, T. Xia, and S. Liu. 2015. “Crucial Role of Lateral Size for Graphene Oxide in Activating Macrophages and Stimulating Pro-Inflammatory Responses in Cells and Animals.” ACS Nano 9 (10): 10498–10515.
   PubMed Web of Science ®Google Scholar
• Maingrette, F., L. Li, and G. Renier. 2008. “C-Reactive Protein Enhances Macrophage Lipoprotein Lipase Expression.” Journal of Lipid Research 49 (9): 1926–1935.
   PubMed Web of Science ®Google Scholar
• Mann, M. 2014. “Fifteen Years of Stable Isotope Labeling by Amino Acids in Cell Culture (SILAC).” Methods in Molecular Biology (Clifton, N.J.) 1188:1–7.
   PubMedGoogle Scholar
• Mizushima, N. 2007. “Autophagy: process and Function.” Genes & Development 21 (22): 2861–2873.
   PubMed Web of Science ®Google Scholar
• Mukherjee, S. P., K. Kostarelos, and B. A. Fadeel. 2018. “Cytokine Profiling of Primary Human Macrophages Exposed to Endotoxin-Free Graphene Oxide: Size-Independent NLRP3 Inflammasome Activation. LID - 10.1002/Adhm.201700815.” Advanced Healthcare Materials 7 (4): 1700815.
   Web of Science ®Google Scholar
• Mukherjee, S. P., B. Lazzaretto, K. Hultenby, L. Newman, A. F. Rodrigues, N. Lozano, K. Kostarelos, P. Malmberg, and B. Fadeel. 2018. “Graphene Oxide Elicits Membrane Lipid Changes and Neutrophil Extracellular Trap Formation.” Chem 4 (2): 334–358.
   Web of Science ®Google Scholar
• Omali, N. B., L. N. Subbaraman, C. Coles-Brennan, Z. Fadli, and L. W. Jones. 2015. “Biological and Clinical Implications of Lysozyme Deposition on Soft Contact Lenses.” Optometry and Vision Science: Official Publication of the American Academy of Optometry 92 (7): 750–757.
   PubMed Web of Science ®Google Scholar
• Ong, S.-E., B. Blagoev, I. Kratchmarova, D. B. Kristensen, H. Steen, A. Pandey, and M. Mann. 2002. “Stable Isotope Labeling by Amino Acids in Cell Culture, SILAC, as a Simple and Accurate Approach to Expression Proteomics.” Molecular & Cellular Proteomics 1 (5): 376–386.
   PubMed Web of Science ®Google Scholar
• Peyron, P.,. C. Bordier, E. N. N'Diaye, and I. Maridonneau-Parini. 2000. “Nonopsonic Phagocytosis of Mycobacterium kansasii by Human Neutrophils Depends on Cholesterol and Is Mediated by CR3 Associated with Glycosylphosphatidylinositol-Anchored Proteins.” The Journal of Immunology (Baltimore, Md.: 1950) 165 (9):5186–5191.
   PubMed Web of Science ®Google Scholar
• Pomyen, Y., M. Segura, T. M. Ebbels, and H. C. Keun. 2015. “Over-Representation of Correlation Analysis (ORCA): a Method for Identifying Associations between Variable Sets.” Bioinformatics (Oxford, England) 31 (1): 102–108.
   PubMed Web of Science ®Google Scholar
• Puissant, A., N. Fenouille, and P. Auberger. 2012. “When Autophagy Meets Cancer through p62/SQSTM1.” American Journal of Cancer Research 2 (4): 397–413.
   PubMed Web of Science ®Google Scholar
• Qu, G., S. Liu, S. Zhang, L. Wang, X. Wang, B. Sun, N. Yin., et al. 2013. “Graphene Oxide Induces Toll-like Receptor 4 (TLR4)-Dependent Necrosis in Macrophages.” ACS Nano 7 (7): 5732–5745.
   PubMed Web of Science ®Google Scholar
• Renier, G., A. C. Desfaits, A. Lambert, and R. Mikhail. 1996. “Role of Oxidant Injury on Macrophage Lipoprotein Lipase (LPL) Production and Sensitivity to LPL.” Journal of Lipid Research 37 (4): 799–809.
   PubMed Web of Science ®Google Scholar
• Renier, G., E. Skamene, J. B. DeSanctis, and D. Radzioch. 1994. “Induction of Tumor Necrosis Factor Alpha Gene Expression by Lipoprotein Lipase.” Journal of Lipid Research 35 (2): 271–278.
   PubMed Web of Science ®Google Scholar
• Russier, J., E. Treossi, A. Scarsi, F. Perrozzi, H. Dumortier, L. Ottaviano, M. Meneghetti, et. al. 2013. “Evidencing the Mask Effect of Graphene Oxide: A Comparative Study on Primary Human and Murine Phagocytic Cells.” Nanoscale 5 (22): 11234–11247.
   PubMed Web of Science ®Google Scholar
• Saeboe-Larssen, S.,. M. Lyamouri, J. Merriam, M. P. Oksvold, and A. Lambertsson. 1998. “Ribosomal Protein Insufficiency and the Minute Syndrome in Drosophila: A Dose-Response Relationship.” Genetics 148 (3): 1215–1224.
   PubMed Web of Science ®Google Scholar
• Scherz-Shouval, R., E. Shvets, E. Fass, H. Shorer, L. Gil, and Z. Elazar. 2007. “Reactive Oxygen Species Are Essential for Autophagy and Specifically Regulate the Activity of Atg4.” The Embo Journal 26 (7): 1749–1760.
   PubMed Web of Science ®Google Scholar
• Seabra, A. B., A. J. Paula, L. R. De, O. L. Alves, and N. Duran. 2014. “Nanotoxicity of Graphene and Graphene Oxide.” Chemical Research in Toxicology 27 (2): 159–168.
   PubMed Web of Science ®Google Scholar
• Shih, C. J., S. Lin, R. Sharma, M. S. Strano, and D. Blankschtein. 2012. “Understanding the pH-Dependent Behavior of Graphene Oxide Aqueous Solutions: A Comparative Experimental and Molecular Dynamics Simulation Study.” Langmuir 28 (1): 235–241.
   PubMed Web of Science ®Google Scholar
• Sun, X., Z. Liu, K. Welsher, J. T. Robinson, A. Goodwin, S. Zaric, H. Dai, et al. 2008. “Nano-Graphene Oxide for Cellular Imaging and Drug Delivery.” Nano Research 1 (3): 203–212.
   PubMed Web of Science ®Google Scholar
• Tang, L. A., W. C. Lee, H. Shi, E. Y. Wong, A. Sadovoy, S. Gorelik, J. Hobley, C. T. Lim, and K. P. Loh. 2012. “Highly Wrinkled Cross-Linked Graphene Oxide Membranes for Biological and Charge-Storage Applications.” Small (Weinheim an Der Bergstrasse, Germany) 8 (3): 423–431.
   PubMed Web of Science ®Google Scholar
• Tatti, M., M. Motta, S. Di Bartolomeo, S. Scarpa, V. Cianfanelli, F. Cecconi, R. Salvioli, et al. 2012. “Reduced Cathepsins B and D Cause Impaired Autophagic Degradation That Can Be Almost Completely Restored by Overexpression of These Two Proteases in Sap C-Deficient Fibroblasts.” Human Molecular Genetics 21 (23): 5159–5173.
   PubMed Web of Science ®Google Scholar
• Torsteinsdottir, I., L. Hakansson, R. Hallgren, B. Gudbjornsson, N. G. Arvidson, and P. Venge. 1999. “Serum Lysozyme: A Potential Marker of Monocyte/Macrophage Activity in Rheumatoid Arthritis.” Rheumatology (Oxford, England) 38 (12): 1249–1254.
   PubMed Web of Science ®Google Scholar
• Uto, T., T. Akagi, K. Yoshinaga, M. Toyama, M. Akashi, and M. Baba. 2011. “The Induction of Innate and Adaptive Immunity by Biodegradable Poly(gamma-Glutamic Acid) Nanoparticles via a TLR4 and MyD88 Signaling Pathway.” Biomaterials 32 (22): 5206–5212.
   PubMed Web of Science ®Google Scholar
• Vianey-Liaud, C., P. Divry, N. Gregersen, and M. Mathieu. 2000. “The Inborn Errors of Mitochondrial Fatty Acid Oxidation.” Critical Reviews in Clinical Laboratory Sciences 37 (1): 1–4.
   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.
   PubMed Web of Science ®Google Scholar
• Wang, S., P. Robinet, J. D. Smith, and K. Gulshan. 2015. “Free-Cholesterol-Mediated Autophagy of ORMDL1 Stimulates Sphingomyelin Biosynthesis.” Autophagy 11 (7): 1207–1208.
   PubMed Web of Science ®Google Scholar
• Warner, J. R. 1999. “The Economics of Ribosome Biosynthesis in Yeast.” Trends in Biochemical Sciences 24 (11): 437–440.
   PubMed Web of Science ®Google Scholar
• Wyatt, E., R. Wu, W. Rabeh, H. W. Park, M. Ghanefar, and H. Ardehali. 1985. “Regulation and Cytoprotective Role of Hexokinase III.” Mechanisms of Ageing and Development 31 (2): 197–212.
   PubMedGoogle 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.
   PubMed Web of Science ®Google Scholar