Characterization of the proteome and lipidome profiles of human lung cells after low dose and chronic exposure to multiwalled carbon nanotubes

References

• Ainaoui, N., F. Hantelys, E. Renaud-Gabardos, M. Bunel, F. Lopez, F. Pujol, R. Planes, et al. 2015. “Promoter-Dependent Translation Controlled by p54nrb and hnRNPM During Myoblast Differentiation.” PLoS One 10 (9): e0136466. doi: 10.1371/journal.pone
   Web of Science ®Google Scholar
• Arnoldussen, Y. J., A. Skogstad, V. Skaug, M. Kasem, A. Haugen, N. Benker, S. Weinbruch, et al. 2015. “Involvement of IL-1 Genes in the Cellular Responses to Carbon Nanotube Exposure.” Cytokine 73 (1): 128–137.
   PubMed Web of Science ®Google Scholar
• Arnoldussen, Y. J, K. H. Anmarkrud, V.Skaug, R. N. Apte, A. Haugen, and S. Zienolddiny. 2016. “Effects of Carbon Nanotubes on Intercellular Communication and Involvement of IL-1 Genes.” Journal of Cell Communication and Signaling 10 (2): 153–162.
   PubMed Web of Science ®Google Scholar
• Artandi, S. E., S. Alson, M. K. Tietze, N. E. Sharpless, S. Ye, R. A. Greenberg, D. H. Castrillon, et al. 2002. “Constitutive Telomerase Expression Promotes Mammary Carcinomas in Aging Mice.” Proceedings of the National Academy of Sciences of the United States of America 99 (12): 8191–8196.
   Web of Science ®Google Scholar
• Atilla-Gokcumen, G. E., E. Muro, J. Relat-Goberna, S. Sasse, A. Bedigian, M. L. Coughlin, Sergi, Garcia-Manyes, et al. 2014. “Dividing Cells Regulate Their Lipid Composition and Localization.” Cell 156 (3): 428–439.
   Web of Science ®Google Scholar
• Bartova, E., B. Malyskova, D. Komurkova, S. Legartova, J. Suchankova, J. Krejci, and S. Kozubek. 2017. “Function of Heterochromatin Protein 1 During DNA Repair.” Protoplasma 254: 1233–1240.
   PubMed Web of Science ®Google Scholar
• Biola-Clier, M., D. Beal, S. Caillat, S. Libert, L. Armand, N. Herlin-Boime, S. Sauvaigo, et al. 2017. “Comparison of the DNA Damage Response in BEAS-2B and A549 Cells Exposed to Titanium Dioxide Nanoparticles.” Mutagenesis 32 (1): 161–172.
   Web of Science ®Google Scholar
• Boström, P., B. Magnusson, P.-A. Svensson, O. Wiklund, J. Borén, L. M. S. Carlsson, M. Ståhlman, S. O. Olofsson, and L. M. Hultén. 2006. “Hypoxia Converts Human Macrophages Into Triglyceride-Loaded Foam Cells.” Arteriosclerosis Thrombosis, and Vascular Biology 26 (8): 1871–1876.
   PubMed Web of Science ®Google Scholar
• Boutet, E., D. Lieberherr, M. Tognolli, M. Schneider, P. Bansal, A. J. Bridge, S. Poux, L. Bougueleret, and I. Xenarios. 2016. “Uniprotkb/Swiss-prot, the Manually Annotated Section of the Uniprot Knowledgebase: How to use the Entry View.” Methods in Molecular Biology 1374: 23–54.
   PubMedGoogle Scholar
• Cadet, J., and J. R. Wagner. 2013. “DNA Base Damage by Reactive Oxygen Species, Oxidizing Agents, and UV Radiation.” Cold Spring Harbor Perspectives in Biology 5 (2): a012559.
   Web of Science ®Google Scholar
• Cao, Y., N. R. Jacobsen, P. H. Danielsen, A. G. Lenz, T. Stoeger, S. Loft, H. Wallin, M. Roursgaard, L. Mikkelsen, and P. Møller. 2014a. “Vascular Effects of Multiwalled Carbon Nanotubes in Dyslipidemic ApoE-/- Mice and Cultured Endothelial Cells.” Toxicological Sciences 138: 104–116.
   PubMed Web of Science ®Google Scholar
• Cao, Y., M. Roursgaard, P. H. Danielsen, P. Møller, and S. Loft. 2014b. “Carbon Black Nanoparticles Promote Endothelial Activation and Lipid Accumulation in Macrophages Independently of Intracellular ROS Production.” PLoS One 9: e106711.
   PubMed Web of Science ®Google Scholar
• Cao, Y., M. Roursgaard, N. R. Jacobsen, P. Møller, and S. Loft. 2016. “Monocyte Adhesion Induced by Multi-walled Carbon Nanotubes and Palmitic Acid in Endothelial Cells and Alveolar–endothelial Co-cultures.” Nanotoxicology 10: 235–244.
   PubMed Web of Science ®Google Scholar
• Cox, J., and M. Mann. 2008. “MaxQuant Enables High Peptide Identification Rates, Individualized p.p.b.-range Mass Accuracies and Proteome-wide Protein Quantification.” Nature Biotechnology 26 (12): 1367–1372.
   PubMed Web of Science ®Google Scholar
• De Volder, M. F. L., S. H. Tawfick, R. H. Baughman, and A. J. Hart. 2013. “Carbon Nanotubes: Present and Future Commercial Applications.” Science 6119: 339.
   PubMed Web of Science ®Google Scholar
• Demir, E., H. Akça, F. Turna, S. Aksakal, D. Burgucu, B. Kaya, O. Tokgün, et al. 2015. “Genotoxic and Cell-transforming Effects of Titanium Dioxide Nanoparticles.” Environmental Research 136: 300–308.
   PubMed Web of Science ®Google Scholar
• Donaldson, K., C. A. Poland, F. A. Murphy, M. Macfarlane, T. Chernova, and A. Schinwald. 2013. “Pulmonary Toxicity of Carbon Nanotubes and Asbestos: Similarities and Differences.” Advanced Drug Delivery Reviews 65 (15): 2078–2086.
   Google Scholar
• Dubois, T., O. Paléotti, A. A. Mironov, V. Fraisier, T. E. B. Stradal, M. A. De Matteis, M. Franco, et al. 2005. “Golgi-localized GAP for Cdc42 Functions Downstream of ARF1 to Control Arp2/3 Complex and F-actin Dynamics.” Nature Cell Biology 7 (4): 353–364.
   Google Scholar
• Galbraith, M. D., M. A. Allen, C. L. Bensard, X. Wang, M. K. Schwinn, B. Qin, H. W. Long, et al. 2013. “HIF1A Employs CDK8-mediator to Stimulate RNAPII Elongation in Response to Hypoxia.” Cell 153 (6): 1327–1339.
   PubMed Web of Science ®Google Scholar
• Grosse, Y., Loomis, D., Guyton, K. Z., Lauby-Secretan, B., El Ghissassi, F., Bouvard, V., et al. 2014. “Carcinogenicity of Fluoro-edenite, Silicon Carbide Fibres and Whiskers, and Carbon Nanotubes.” Lancet Oncology 15: 1427–1428.
   PubMed Web of Science ®Google Scholar
• Gursoy-Yuzugullu, O., N. House, and B. D. Price. 2016. “Patching Broken DNA: Nucleosome Dynamics and the Repair of DNA Breaks.” The Journal of Molecular Biology 428 (9 Pt B): 1846–1860.
   Google Scholar
• Haniu, H., Y. Matsuda, K. Takeuchi, Y. A. Kim, T. Hayashi, and M. Endo. 2010. “Proteomics-based Safety Evaluation of Multi-walled Carbon Nanotubes.” Toxicology and Applied Pharmacology 242 (3): 256–262.
   PubMed Web of Science ®Google Scholar
• Herzog, R., K. Schuhmann, D. Schwudke, J. L. Sampaio, S. R. Bornstein, M. Schroeder, A. Shevchenko, et al. 2012. “LipidXplorer: A Software for Consensual Cross-platform Lipidomics.” PLoS One 7 (1): e29851.
   PubMed Web of Science ®Google Scholar
• Hilton, G. M., A. J. Taylor, C. D. Mcclure, G. N. Parsons, J. C. Bonner, and M. S. Bereman. 2015. “Toxicoproteomic Analysis of Pulmonary Carbon Nanotube Exposure Using LC-MS/MS.” Toxicology 329: 80–87.
   PubMed Web of Science ®Google Scholar
• Hilton, G. M., A. J. Taylor, S. Hussain, E. C. Dandley, E. H. Griffith, S. Garantziotis, G. N. Parsons, et al. 2017. “Mapping Differential Cellular Protein Response of Mouse Alveolar Epithelial Cells to Multi-walled Carbon Nanotubes as a Function of Atomic Layer Deposition Coating.” Nanotoxicology 11 (3): 313–326.
   PubMed Web of Science ®Google Scholar
• Ho, H. Y., R. Rohatgi, A. M. Lebensohn, M. Le, J. Li, S. P. Gygi, and M. W. Kirschner. 2004. “Toca-1 Mediates Cdc42-Dependent Actin Nucleation by Activating the N-WASP-WIP Complex.” Cell 118: 203–216.
   PubMed Web of Science ®Google Scholar
• Hovhannisyan, R. H., and R. P. Carstens. 2007. “Heterogeneous Ribonucleoprotein m is a Splicing Regulatory Protein that can Enhance or Silence Splicing of Alternatively Spliced Exons.” The Journal of Biological Chemistry 282 (50): 36265–36274.
   Google Scholar
• Huang, J., Z. Gong, G. Ghosal, and J. Chen. 2009. “SOSS Complexes Participate in the Maintenance of Genomic Stability.” Molecular Cell 35 (3):384–393.
   PubMed Web of Science ®Google Scholar
• Iannilli, F., F. Zalfa, A. Gartner, C. Bagni, C. G. Dotti, F. Di Cunto, 2013. “Cytoplasmic TERT Associates to RNA Granules in Fully Mature Neurons: Role in the Translational Control of the Cell Cycle Inhibitor p15INK4B. PLoS One 8 (6): e66602.
   PubMed Web of Science ®Google Scholar
• Iijima, S. 1991. “Helical Microtubules of Graphitic Carbon.” Nature 354 (6348): 56–58.
   Web of Science ®Google Scholar
• Jackson, S. P., and D. Durocher. 2013. “Regulation of DNA Damage Responses by Ubiquitin and SUMO.” Molecular Cell 49 (5): 795–807.
   PubMed Web of Science ®Google Scholar
• Jensen, K. A., Y. Kembouche, E. Christiansen, N. R. Jacobsen, H. Wallin, C. Guiot, O. Spalla, and O. Witschger. 2011. “The generic NANOGENOTOX dispersion protocol.” Standard Operation Procedure (SOP) and background documentation Final Protocol for producing suitable manufactured nanomaterial exposure media.
   Google Scholar
• Jia, X., and F. Wei. 2017. “Advances in Production and Applications of Carbon Nanotubes.” Topics in Current Chemistry (Cham) 375:18.
   Google Scholar
• Ju, L., G. Zhang, X. Zhang, Z. Jia, X. Gao, Y. Jiang, C. Yan, et al. 2014. “Proteomic Analysis of Cellular Response Induced by Multi-Walled Carbon Nanotubes Exposure in A549 Cells.” PLoS One 9 (1): e84974.
   PubMed Web of Science ®Google Scholar
• Kasai, T., Y. Umeda, M. Ohnishi, H. Kondo, T. Takeuchi, S. Aiso, T. Nishizawa, et al. 2015. “Thirteen-week Study of Toxicity of Fiber-like Multi-walled Carbon Nanotubes with Whole-body Inhalation Exposure in Rats.” Nanotoxicology 9 (4): 413–422.
   PubMed Web of Science ®Google Scholar
• Kato, T., Y. Totsuka, K. Ishino, Y. Matsumoto, Y. Tada, D. Nakae, S. Goto, , et al. 2013. “Genotoxicity of Multi-walled Carbon Nanotubes in Both In vitro and In vivo Assay Systems.” Nanotoxicology 7 (4): 452–461.
   PubMed Web of Science ®Google Scholar
• Kil, Y. J., C. Becker, W. Sandoval, D. Goldberg, and M. Bern. 2011. “Preview: A Program for Surveying Shotgun Proteomics Tandem Mass Spectrometry Data.” Analytical Chemistry 83 (13): 5259–5267.
   PubMed Web of Science ®Google Scholar
• Li, Z., R. J. Schulze, S. G. Weller, E. W. Krueger, M. B. Schott, X. Zhang, C. A. Casey, et al. 2016. A Novel Rab10-EHBP1-EHD2 Complex Essential for the Autophagic Engulfment of Lipid Droplets.” Science Advances 2 (12): e1601470.
   PubMed Web of Science ®Google Scholar
• Luo, Z., C. Lin, and A. Shilatifard. 2012. “The Super Elongation Complex (SEC) Family in Transcriptional Control.” Nature Reviews Molecular Cell Biology 13 (9): 543–547.
   Google Scholar
• Maruyama, K., H. Haniu, N. Saito, Y. Matsuda, T. Tsukahara, S. Kobayashi, M. Tanaka, et al. 2015. “Endocytosis of Multiwalled Carbon Nanotubes in Bronchial Epithelial and Mesothelial Cells.” BioMed Research International 2015: 793186.
   Google Scholar
• Muller, J., F. Huaux, N. Moreau, P. Misson, J. -F. Heilier, M. Delos, M. Arras, et al. 2005. “Respiratory Toxicity of Multi-wall Carbon Nanotubes.” Toxicology and Applied Pharmacology 207 (3): 221–231.
   Google Scholar
• Muro, E., G. E. Atilla-Gokcumen, and U. S. Eggert. 2014. “Lipids in Cell Biology: How can we Understand them Better? Molecular Biology of the Cell 25 (12): 1819–1823.
   PubMed Web of Science ®Google Scholar
• Nagai, H., Y. Okazaki, S. H. Chew, N. Misawa, Y. Yamashita, S. Akatsuka, T. Ishihara, et al. 2011. “Diameter and Rigidity of Multiwalled Carbon Nanotubes are Critical Factors in Mesothelial Injury and Carcinogenesis.” Proceedings of the National Academy of Sciences of the United States of America 108 (9): E1330–E1338.
   Google Scholar
• Paquet, N., M. N. Adams, N. W. Ashton, C. Touma, R. Gamsjaeger, L. Cubeddu, V. Leong, et al. 2016. “hSSB1 (NABP2/OBFC2B) is Regulated by Oxidative Stress.” Scientific Reports 6: 27446.
   Google Scholar
• Poland, C. A., R. Duffin, I. Kinloch, A. Maynard, W. A. H. Wallace, A. Seaton, V. Stone, et al. 2008. “Carbon Nanotubes Introduced into the Abdominal Cavity of Mice Show Asbestos-like Pathogenicity in a Pilot Study.” Nature Nanotechnology 3: 423–428.
   Google Scholar
• Polimeni, M., G. R. Gulino, E. Gazzano, J. Kopecka, A. Marucco, I. Fenoglio, F. Cesano, et al. 2015. “Multi-walled Carbon Nanotubes Directly Induce Epithelial-mesenchymal Transition in Human Bronchial Epithelial Cells via the TGF-β-Mediated Akt/GSK-3β/SNAIL-1 Signalling Pathway.” Particle and Fibre Toxicology 13 (1): 27.
   Google Scholar
• Ravichandran, P., S. Baluchamy, B. Sadanandan, R. Gopikrishnan, S. Biradar, V. Ramesh, J. C. Hall, et al. 2010. “Multiwalled Carbon Nanotubes Activate NF-κB and AP-1 Signaling Pathways to Induce Apoptosis in Rat Lung Epithelial Cells.” Apoptosis 15 (12): 1507–1516.
   PubMed Web of Science ®Google Scholar
• Richard, D. J., E. Bolderson, L. Cubeddu, R. I. M. Wadsworth, K. Savage, G. G. Sharma, M. L. Nicolette, et al. 2008. “Single-stranded DNA-Binding Protein hSSB1 is Critical for Genomic Stability.” Nature 453 (7195): 677–681.
   PubMed Web of Science ®Google Scholar
• Rittinghausen, S., A. Hackbarth, O. Creutzenberg, H. Ernst, U. Heinrich, A. Leonhardt, D. Schaudien, et al. 2014. “The Carcinogenic Effect of Various Multi-walled Carbon Nanotubes (MWCNTs) After Intraperitoneal Injection in Rats.” Particle and Fibre Toxicology 11 (1): 59.
   PubMedGoogle Scholar
• Rosenblat, M., N. Volkova, N. Paland, and M. Aviram. 2012. “Triglyceride Accumulation in Macrophages Upregulates Paraoxonase 2 (PON2) Expression via ROS-Mediated JNK/c-Jun Signaling Pathway Activation.” BioFactors 38 (6): 458–469.
   PubMed Web of Science ®Google Scholar
• Sarangi, P., and X. Zhao. 2015. “SUMO-mediated Regulation of DNA Damage Repair and Responses.” Trends in Biochemical Sciences 40 (4): 233–242.
   Google Scholar
• Sargent, L. M, D. W. Porter, L. M. Staska, A. F. Hubbs, D. T. Lowry, L. Battelli, K. J. Siegrist, et al. 2014. “Promotion of Lung Adenocarcinoma Following Inhalation Exposure to Multi-walled Carbon Nanotubes.” Particle and Fibre Toxicology 11 (1): 3.
   Google Scholar
• Schuhmann, K., R. Almeida, M. Baumert, R. Herzog, S. R. Bornstein, and A. Shevchenko. 2012. “Shotgun Lipidomics on a LTQ Orbitrap Mass Spectrometer by Successive Switching Between Acquisition Polarity Modes.” Journal of Mass Spectrometry 47 (1): 96–104.
   PubMed Web of Science ®Google Scholar
• Semenza, G. L. 2007. “Oxygen-dependent Regulation of Mitochondrial Respiration by Hypoxia-inducible Factor 1. Biochemical Journal 405 (1): 1–9.
   PubMedGoogle Scholar
• Singhapol, C., D. Pal, R. Czapiewski, M. Porika, G. Nelson, G. C. Saretzki, J. Santos, 2013. “Mitochondrial Telomerase Protects Cancer Cells from Nuclear DNA Damage and Apoptosis.” PLoS One 8 (1): e52989.
   PubMed Web of Science ®Google Scholar
• Snyder, R. J., S. Hussain, A. B. Rice, and S. Garantziotis. 2014. “Multiwalled Carbon Nanotubes Induce Altered Morphology and Loss of Barrier Function in Human Bronchial Epithelium at Noncytotoxic Doses.” International Journal of Nanomedicine 9: 4093–4105.
   Google Scholar
• Srivastava, R. K, A. B. Pant, M. P. Kashyap, V. Kumar, M. Lohani, L. Jonas, Q. Rahman, 2011. “Multi-walled Carbon Nanotubes Induce Oxidative Stress and Apoptosis in Human Lung Cancer Cell Line-A549. Nanotoxicology 5 (2): 195–207.
   PubMed Web of Science ®Google Scholar
• Stankovic-Valentin, N., K. Drzewicka, C. Konig, E. Schiebel, and F. Melchior. 2016. “Redox Regulation of SUMO Enzymes is Required for ATM Activity and Survival in Oxidative Stress.” EMBO Journal 35 (12): 1312–1329.
   Google Scholar
• Switzeny, O. J., E. Müllner, R. K. H. Wagne, H. Brath, E. Aumüller, and A. G. Haslberger. 2012. “Vitamin and Antioxidant Rich Diet Increases MLH1 Promoter DNA Methylation in DMT2 Subjects.” Clinical Epigenetics 4 (1): 19.
   Google Scholar
• Tsukahara, T., and H. Haniu. 2011. “Nanoparticle-mediated Intracellular Lipid Accumulation During C2C12 Cell Differentiation.” Biochemical and Biophysical Research Communications 406 (4): 558–563.
   PubMed Web of Science ®Google Scholar
• Ursini, C. L., D. Cavallo, A. M. Fresegna, A. Ciervo, R. Maiello, G. Buresti, S. Casciardi, S. Bellucci, and S. Iavicoli. 2014. “Differences in Cytotoxic, Genotoxic, and Inflammatory Response of Bronchial and Alveolar Human Lung Epithelial Cells to Pristine and COOH-Functionalized Multiwalled Carbon Nanotubes.” BioMed Research International 2014: 359506.
   Google Scholar
• Vidanapathirana, A. K., X. Lai, S. C. Hilderbrand, J. E. Pitzer, R. Podila, S J. Sumner, T. R. Fennell, C. J. Wingard, F. A. Witzmann, J. M. Brown, 2012. “Multi-walled Carbon Nanotube Directed Gene and Protein Expression in Cultured Human Aortic Endothelial Cells is Influenced by Suspension Medium.” Toxicology 302 (2–3): 114–122.
   PubMed Web of Science ®Google Scholar
• Wang, L., T. A. Stueckle, A. Mishra, R. Derk, T. Meighan, V. Castranova, Y. Rojanasakul, 2014. “Neoplastic-like Transformation Effect of Single-walled and Multi-walled Carbon Nanotubes Compared to Asbestos on Human Lung Small Airway Epithelial Cells.” Nanotoxicology 8 (5): 485–507.
   PubMed Web of Science ®Google Scholar
• Wang, X., J. Guo, T. Chen, H. Nie, H. Wang, J. Zang, X. Cui, G. Jia, 2012. “Multi-walled Carbon Nanotubes Induce Apoptosis via Mitochondrial Pathway and Scavenger Receptor.” Toxicology In Vitro 26 (6): 799–806.
   PubMed Web of Science ®Google Scholar
• Watson, J. R., H. M. Fox, D. Nietlispach, J. L. Gallop, D. Owen, and H. R. Mott. 2016. “Investigation of the Interaction Between Cdc42 and its Effector TOCA1: Handover of Cdc42 to the Actin Regulator n-wasp is Facilitated by Differential Binding Affinities.” The Journal of Biological Chemistry 291: 13875–13890.
   Google Scholar
• Wick, P., P. Manser, L. Limbach, U. Dettlaffweglikowska, F. Krumeich, S. Roth, W. Stark, and A. Bruinink. 2007. “The Degree and Kind of Agglomeration Affect Carbon Nanotube Cytotoxicity.” Toxicology Letters 168 (2): 121–131.
   PubMed Web of Science ®Google Scholar
• Witzmann, F. A., and N. A. Monteiro-Riviere. 2006. “Multi-walled Carbon Nanotube Exposure Alters Protein Expression in Human Keratinocytes.” Nanomedicine: Nanotechnology, Biology and Medicine 2 (3): 158–168.
   PubMed Web of Science ®Google Scholar
• Xu, J., D. B. Alexander, M. Futakuchi, T. Numano, K. Fukamachi, M. Suzui, T. Omori, et al. 2014. “Size- and Shape-dependent Pleural Translocation, Deposition, Fibrogenesis, and Mesothelial Proliferation by Multiwalled Carbon Nanotubes.” Cancer Science 105 (7): 763–769.
   PubMed Web of Science ®Google Scholar
• Xu, J., M. Futakuchi, H. Shimizu, D. B. Alexander, K. Yanagihara, K. Fukamachi, M. Suzui, et al. 2012. “Multi-walled Carbon Nanotubes Translocate into the Pleural Cavity and Induce Visceral Mesothelial Proliferation in Rats.” Cancer Science 103 (12): 2045–2050.
   PubMed Web of Science ®Google Scholar
• Zhu, Q., S. Ghoshal, R. Tyagi, and A. Chakraborty. 2017. “Global IP6K1 Deletion Enhances Temperature Modulated Energy Expenditure Which Reduces Carbohydrate and Fat Induced Weight Gain.” Molecular Metabolism 16: 73–85.
   PubMed Web of Science ®Google Scholar