Multi-walled carbon nanotubes upregulate mitochondrial gene expression and trigger mitochondrial dysfunction in primary human bronchial epithelial cells

References

• Ali, A., M. Suhail, S. Mathew, M. A. Shah, S. M. Harakeh, S. Ahmad, Z. Kazmi, et al. 2016. “Nanomaterial Induced Immune Responses and Cytotoxicity.” Journal of Nanoscience and Nanotechnology 16 (1): 40–57. doi:10.1166/jnn.2016.10885.
   Google Scholar
• Bai, W., Z. Wu, S. Mitra, and J. M. Brown. 2016. “Effects of Multiwalled Carbon Nanotube Surface Modification and Purification on Bovine Serum Albumin Binding and Biological Responses.” Journal of Nanomaterials 2016: 1. doi:10.1155/2016/2159537.
   Web of Science ®Google Scholar
• Bai, Y., R. Zhang, X. Ye, Z. Zhu, H. Xie, B. Shen, D. Cai, et al. 2018. “Carbon Nanotube Bundles with Tensile Strength over 80 GPa.” Nature Nanotechnology 13 (7): 589–595.
   PubMed Web of Science ®Google Scholar
• Baughman, R. H., A. A. Zakhidov, and W. A. de Heer. 2002. “Carbon Nanotubes – The Route toward Applications.” Science 297 (5582): 787–792. doi:10.1126/science.1060928.
   PubMed Web of Science ®Google Scholar
• Bianco, A., K. Kostarelos, and M. Prato. 2005. “Applications of Carbon Nanotubes in Drug Delivery.” Current Opinion in Chemical Biology 9 (6): 674–679. doi:10.1016/j.cbpa.2005.10.005.
   PubMed Web of Science ®Google Scholar
• Bibb, M. J., R. A. Van Etten, C. T. Wright, M. W. Walberg, and D. A. Clayton. 1981. “Sequence and Gene Organization of Mouse Mitochondrial DNA.” Cell 26 (2 Pt 2): 167–180. doi:10.1016/0092-8674(81)90300-7.
   PubMed Web of Science ®Google Scholar
• Birch, M. E. 2011. “Exposure and Emissions Monitoring during Carbon Nanofiber Production–Part II: Polycyclic Aromatic Hydrocarbons.” The Annals of Occupational Hygiene 55 (9): 1037–1047. doi:10.1093/annhyg/mer070.
   PubMedGoogle Scholar
• Bossi, E., D. Zanella, R. Gornati, and G. Bernardini. 2016. “Cobalt Oxide Nanoparticles Can Enter inside the Cells by Crossing Plasma Membranes.” Scientific Reports 6 (1): 22254. doi:10.1038/srep22254.
   PubMed Web of Science ®Google Scholar
• Boyles, M. S., L. Young, D. M. Brown, L. MacCalman, H. Cowie, A. Moisala, F. Smail, et al. 2015. “Multi-Walled Carbon Nanotube Induced Frustrated Phagocytosis, Cytotoxicity and Pro-Inflammatory Conditions in Macrophages Are Length Dependent and Greater than That of Asbestos.” Toxicology in Vitro 29 (7): 1513–1528. doi:10.1016/j.tiv.2015.06.012.
   PubMed Web of Science ®Google Scholar
• Braydich-Stolle, L., S. Hussain, J. J. Schlager, and M. C. Hofmann. 2005. “In Vitro Cytotoxicity of Nanoparticles in Mammalian Germline Stem Cells.” Toxicological Sciences 88 (2): 412–419. doi:10.1093/toxsci/kfi256.
   PubMed Web of Science ®Google Scholar
• Cao, Y., M. Roursgaard, N. R. Jacobsen, P. Moller, 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 (2): 235–244. doi:10.3109/17435390.2015.1048325.
   PubMed Web of Science ®Google Scholar
• Costa, P. M., M. Bourgognon, J. T. Wang, and K. T. Al-Jamal. 2016. “Functionalised Carbon Nanotubes: From Intracellular Uptake and Cell-Related Toxicity to Systemic Brain Delivery.” Journal of Controlled Release 241: 200–219. doi:10.1016/j.jconrel.2016.09.033.
   PubMed Web of Science ®Google Scholar
• Dames, S., L. S. Chou, Y. Xiao, T. Wayman, J. Stocks, M. Singleton, K. Eilbeck, and R. Mao. 2013. “The Development of Next-Generation Sequencing Assays for the Mitochondrial Genome and 108 Nuclear Genes Associated with Mitochondrial Disorders.” The Journal of Molecular Diagnostics 15 (4): 526–534. doi:10.1016/j.jmoldx.2013.03.005.
   PubMed Web of Science ®Google Scholar
• De Volder, M. F., S. H. Tawfick, R. H. Baughman, and A. J. Hart. 2013. “Carbon Nanotubes: Present and Future Commercial Applications.” Science 339 (6119): 535–539. doi:10.1126/science.1222453.
   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. doi:10.1016/j.addr.2013.07.014.
   PubMed Web of Science ®Google Scholar
• Donaldson, K., R. Aitken, L. Tran, V. Stone, R. Duffin, G. Forrest, and A. Alexander. 2006. “Carbon Nanotubes: A Review of Their Properties in Relation to Pulmonary Toxicology and Workplace Safety.” Toxicological Sciences 92 (1): 5–22. doi:10.1093/toxsci/kfj130.
   PubMed Web of Science ®Google Scholar
• Du Choi, S., D. Kim, Y. P. Kang, and D. H. Jang. 2012. “Effect of Spray Process Conditions on Uniformity of Carbon Nanotube Thin Films.” Journal of Nanoscience and Nanotechnology 12 (7): 5290–5296. doi:10.1166/jnn.2012.6267.
   PubMed Web of Science ®Google Scholar
• Du, J., C. Ge, Y. Liu, R. Bai, D. Li, Y. Yang, L. Liao, and C. Chen. 2011. “The Interaction of Serum Proteins with Carbon Nanotubes Depend on the Physicochemical Properties of Nanotubes.” Journal of Nanoscience and Nanotechnology 11 (11): 10102–10110. doi:10.1166/jnn.2011.4976.
   PubMed Web of Science ®Google Scholar
• Garcia-Hevia, L., F. Fernandez, C. Gravalos, A. Garcia, J. C. Villegas, and M. L. Fanarraga. 2014. “Nanotube Interactions with Microtubules: Implications for Cancer Medicine.” Nanomedicine (Nanomedicine) 9 (10): 1581–1588. doi:10.2217/nnm.14.92.
   PubMed Web of Science ®Google Scholar
• Garcia-Hevia, L., J. C. Villegas, F. Fernandez, I. Casafont, J. Gonzalez, R. Valiente, and M. L. Fanarraga. 2016. “Multiwalled Carbon Nanotubes Inhibit Tumor Progression in a Mouse Model.” Advanced Healthcare Materials 5 (9): 1080–1087. doi:10.1002/adhm.201500753.
   PubMed Web of Science ®Google Scholar
• Hauswirth, W. W., and D. A. Clayton. 1985. “Length Heterogeneity of a Conserved Displacement-Loop Sequence in Human Mitochondrial DNA.” Nucleic Acids Research 13 (22): 8093–8104. doi:10.1093/nar/13.22.8093.
   PubMed Web of Science ®Google Scholar
• He, X. Q., S. H. Young, D. Schwegler-Berry, W. P. Chisholm, J. E. Fernback, and Q. Ma. 2011. “Multiwalled Carbon Nanotubes Induce a Fibrogenic Response by Stimulating Reactive Oxygen Species Production, Activating NF-Kappa B Signaling, and Promoting Fibroblast-to-Myofibroblast Transformation.” Chemical Research in Toxicology 24 (12): 2237–2248. doi:10.1021/tx200351d.
   PubMed Web of Science ®Google Scholar
• Hecht, D. S., L. Hu, and G. Irvin. 2011. “Emerging Transparent Electrodes Based on Thin Films of Carbon Nanotubes, Graphene, and Metallic Nanostructures.” Advanced Materials 23 (13): 1482–1513. doi:10.1002/adma.201003188.
   PubMed Web of Science ®Google Scholar
• Hirose, M., P. Schilf, Y. Gupta, K. Zarse, A. Kunstner, A. Fahnrich, H. Busch, et al. 2018. “Low-Level Mitochondrial Heteroplasmy Modulates DNA Replication, Glucose Metabolism and Lifespan in Mice.” Scientific Reports 8 (1): 5872.
   PubMedGoogle Scholar
• Hodgkinson, A., Y. Idaghdour, E. Gbeha, J. C. Grenier, E. Hip-Ki, V. Bruat, J. P. Goulet, T. de Malliard, and P. Awadalla. 2014. “High-Resolution Genomic Analysis of Human Mitochondrial RNA Sequence Variation.” Science 344 (6182): 413–415. doi:10.1126/science.1251110.
   PubMed Web of Science ®Google Scholar
• Hussain, S., S. Sangtian, S. M. Anderson, R. J. Snyder, J. D. Marshburn, A. B. Rice, J. C. Bonner, and S. Garantziotis. 2014. “Inflammasome Activation in Airway Epithelial Cells after Multi-Walled Carbon Nanotube Exposure Mediates a Profibrotic Response in Lung Fibroblasts.” Particle and Fibre Toxicology 11 (1): 28. doi:10.1186/1743-8977-11-28.
   PubMedGoogle Scholar
• Kagan, V. E., J. Jiang, Z. Huang, Y. Y. Tyurina, C. Desbourdes, C. Cottet-Rousselle, H. H. Dar, et al. 2016. “NDPK-D (NM23-H4)-Mediated Externalization of Cardiolipin Enables Elimination of Depolarized Mitochondria by Mitophagy.” Cell Death & Differentiation 23 (7): 1140–1151. doi:10.1038/cdd.2015.160.
   PubMed Web of Science ®Google Scholar
• Kang, B., S. Chang, Y. Dai, D. Yu, and D. Chen. 2010. “Cell Response to Carbon Nanotubes: Size-Dependent Intracellular Uptake Mechanism and Subcellular Fate.” Small 6 (21): 2362–2366. doi:10.1002/smll.201001260.
   PubMed Web of Science ®Google Scholar
• Khoor, A., M. T. Stahlman, M. E. Gray, and J. A. Whitsett. 1994. “Temporal-Spatial Distribution of SP-B and SP-C Proteins and mRNAs in Developing Respiratory Epithelium of Human Lung.” Journal of Histochemistry & Cytochemistry 42 (9): 1187–1199. doi:10.1177/42.9.8064126.
   PubMed Web of Science ®Google Scholar
• Kim, I., and J. J. Lemasters. 2011. “Mitophagy Selectively Degrades Individual Damaged Mitochondria after Photoirradiation.” Antioxidants & Redox Signaling 14 (10): 1919–1928. doi:10.1089/ars.2010.3768.
   PubMed Web of Science ®Google Scholar
• Lam, C. W., J. T. James, R. McCluskey, and R. L. Hunter. 2003. “Pulmonary Toxicity of Single-Wall Carbon Nanotubes in Mice 7 and 90 Days after Intratracheal Instillation.” Toxicological Sciences 77 (1): 126–134. doi:10.1093/toxsci/kfg243.
   PubMed Web of Science ®Google Scholar
• Lan, J., N. Gou, C. Gao, M. He, and A. Z. Gu. 2014. “Comparative and Mechanistic Genotoxicity Assessment of Nanomaterials via a Quantitative Toxicogenomics Approach across Multiple Species.” Environmental Science & Technology 48 (21): 12937–12945. doi:10.1021/es503065q.
   PubMed Web of Science ®Google Scholar
• Law, M., J. Goldberger, and P. D. Yang. 2004. “Semiconductor Nanowires and Nanotubes.” Annual Review of Materials Research 34 (1): 83–122. doi:10.1146/annurev.matsci.34.040203.112300.
   Google Scholar
• Liang, X. J., C. Chen, Y. Zhao, L. Jia, and P. C. Wang. 2008. “Biopharmaceutics and Therapeutic Potential of Engineered Nanomaterials.” Current Drug Metabolism 9 (8): 697–709. doi:10.2174/138920008786049230.
   PubMed Web of Science ®Google Scholar
• Liu, X., and Z. Chen. 2017. “The Pathophysiological Role of Mitochondrial Oxidative Stress in Lung Diseases.” Journal of Translational Medicine 15 (1): 207. doi:10.1186/s12967-017-1306-5.
   PubMedGoogle Scholar
• Manke, A., L. Wang, and Y. Rojanasakul. 2013. “Mechanisms of Nanoparticle-Induced Oxidative Stress and Toxicity.” Biomed Research International 2013: 1. doi:10.1155/2013/942916.
   Web of Science ®Google Scholar
• Matson, C. W., M. M. Lambert, T. J. McDonald, R. L. Autenrieth, K. C. Donnelly, A. Islamzadeh, D. I. Politov, and J. W. Bickham. 2006. “Evolutionary Toxicology: Population-Level Effects of Chronic Contaminant Exposure on the Marsh Frogs (Rana Ridibunda) of Azerbaijan.” Environmental Health Perspectives 114 (4): 547–552. doi:10.1289/ehp.8404.
   PubMed Web of Science ®Google Scholar
• Minoche, A. E., J. C. Dohm, and H. Himmelbauer. 2011. “Evaluation of Genomic High-Throughput Sequencing Data Generated on Illumina HiSeq and Genome Analyzer Systems.” Genome Biology 12 (11): R112. doi:10.1186/gb-2011-12-11-r112.
   PubMed Web of Science ®Google Scholar
• Morozesk, M., L. S. Franqui, A. S. Mansano, D. S. T. Martinez, and M. N. Fernandes. 2018. “Interactions of Oxidized Multiwalled Carbon Nanotube with Cadmium on Zebrafish Cell Line: The Influence of Two co-Exposure Protocols on in Vitro Toxicity Tests.” Aquatic Toxicology 200: 136–147. doi:10.1016/j.aquatox.2018.05.002.
   PubMed Web of Science ®Google Scholar
• Mu, Q., D. L. Broughton, and B. Yan. 2009. “Endosomal Leakage and Nuclear Translocation of Multiwalled Carbon Nanotubes: Developing a Model for Cell Uptake.” Nano Letters 9 (12): 4370–4375. doi:10.1021/nl902647x.
   PubMed Web of Science ®Google Scholar
• Muller, K., E. Bugnicourt, M. Latorre, M. Jorda, Y. Echegoyen Sanz, J. M. Lagaron, O. Miesbauer, et al. 2017. “Review on the Processing and Properties of Polymer Nanocomposites and Nanocoatings and Their Applications in the Packaging, Automotive and Solar Energy Fields.” Nanomaterials (Nanomaterials) 7 (4). doi:10.3390/nano7040074.
   Google Scholar
• Nanotechnology Consumer Product Inventory. 2019. “The Project on Emerging Nanotechnologies.” Accessed 6 May 2019. http://www.nanotechproject.org/cpi/about/analysis/
   Google Scholar
• Nerl, H. C., C. Cheng, A. E. Goode, S. D. Bergin, B. Lich, M. Gass, and A. E. Porter. 2011. “Imaging Methods for Determining Uptake and Toxicity of Carbon Nanotubes in Vitro and in Vivo.” Nanomedicine 6 (5): 849–865. doi:10.2217/nnm.11.87.
   PubMed Web of Science ®Google Scholar
• Panas, A., A. Comouth, H. Saathoff, T. Leisner, M. Al-Rawi, M. Simon, G. Seemann, et al. 2014. “Silica Nanoparticles Are Less Toxic to Human Lung Cells When Deposited at the Air-Liquid Interface Compared to Conventional Submerged Exposure.” Beilstein Journal of Nanotechnology 5: 1590–1602. doi:10.3762/bjnano.5.171.
   PubMed Web of Science ®Google Scholar
• Park, E. J., J. Roh, S. N. Kim, M. S. Kang, Y. A. Han, Y. Kim, J. T. Hong, and K. Choi. 2011. “A Single Intratracheal Instillation of Single-Walled Carbon Nanotubes Induced Early Lung Fibrosis and Subchronic Tissue Damage in Mice.” Archives of Toxicology 85 (9): 1121–1131. doi:10.1007/s00204-011-0655-8.
   PubMed Web of Science ®Google Scholar
• Rivero, P. J., A. Urrutia, J. Goicoechea, and F. J. Arregui. 2015. “Nanomaterials for Functional Textiles and Fibers.” Nanoscale Research Letters 10 (1): 501. doi:10.1186/s11671-015-1195-6.
   PubMed Web of Science ®Google Scholar
• Rotoli, B. M., O. Bussolati, A. Barilli, P. P. Zanello, M. G. Bianchi, A. Magrini, A. Pietroiusti, A. Bergamaschi, and E. Bergamaschi. 2009. “Airway Barrier Dysfunction Induced by Exposure to Carbon Nanotubes in Vitro: Which Role for Fiber Length?” Human & Experimental Toxicology 28 (6–7): 361–368. doi:10.1177/0960327109105159.
   PubMed Web of Science ®Google Scholar
• Ryman-Rasmussen, J. P., E. W. Tewksbury, O. R. Moss, M. F. Cesta, B. A. Wong, and J. C. Bonner. 2009. “Inhaled Multiwalled Carbon Nanotubes Potentiate Airway Fibrosis in Murine Allergic Asthma.” American Journal of Respiratory Cell and Molecular Biology 40 (3): 349–358. doi:10.1165/rcmb.2008-0276OC.
   PubMed Web of Science ®Google Scholar
• Shukla, A., M. Jung, M. Stern, N. K. Fukagawa, D. J. Taatjes, D. Sawyer, B. Van Houten, and B. T. Mossman. 2003. “Asbestos Induces Mitochondrial DNA Damage and Dysfunction Linked to the Development of Apoptosis.” American Journal of Physiology-Lung Cellular and Molecular Physiology 285 (5): L1018–L1025. doi:10.1152/ajplung.00038.2003.
   PubMed Web of Science ®Google Scholar
• Shvedova, A. A., E. R. Kisin, R. Mercer, A. R. Murray, V. J. Johnson, A. I. Potapovich, Y. Y. Tyurina, et al. 2005. “Unusual Inflammatory and Fibrogenic Pulmonary Responses to Single-Walled Carbon Nanotubes in Mice.” American Journal of Physiology-Lung Cellular and Molecular Physiology 289 (5): L698–L708. doi:10.1152/ajplung.00084.2005.
   PubMed Web of Science ®Google Scholar
• Siegrist, K. J., S. H. Reynolds, M. L. Kashon, D. T. Lowry, C. Dong, A. F. Hubbs, S. H. Young, et al. 2014. “Genotoxicity of Multi-Walled Carbon Nanotubes at Occupationally Relevant Doses.” Particle and Fibre Toxicology 11 (1): 6. doi:10.1186/1743-8977-11-6.
   PubMedGoogle Scholar
• Skandani, A. A., and M. Al-Haik. 2013. “Reciprocal Effects of the Chirality and the Surface Functionalization on the Drug Delivery Permissibility of Carbon Nanotubes.” Soft Matter 9 (48): 11645–11649. doi:10.1039/C3SM52126E.
   PubMed Web of Science ®Google Scholar
• Skonieczna, Katarzyna, Boris Malyarchuk, Arkadiusz Jawień, Andrzej Marszałek, Zbigniew Banaszkiewicz, Paweł Jarmocik, Marcelina Borcz, Piotr Bała, and Tomasz Grzybowski. 2015. “Heteroplasmic Substitutions in the Entire Mitochondrial Genomes of Human Colon Cells Detected by Ultra-Deep 454 Sequencing.” Forensic Science International: Genetics 15: 16–20. doi:10.1016/j.fsigen.2014.10.021.
   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.
   PubMed Web of Science ®Google Scholar
• Snyder, R. J., S. Hussain, C. J. Tucker, S. H. Randell, and S. Garantziotis. 2017. “Impaired Ciliogenesis in Differentiating Human Bronchial Epithelia Exposed to non-Cytotoxic Doses of Multi-Walled Carbon Nanotubes.” Particle and Fibre Toxicology 14 (1): 44. doi:10.1186/s12989-017-0225-1.
   PubMedGoogle Scholar
• Sturm, R. 2016. “A Stochastic Model of Carbon Nanotube Deposition in the Airways and Alveoli of the Human Respiratory Tract.” Inhalation Toxicology 28 (2): 49–60. doi:10.3109/08958378.2015.1136009.
   PubMed Web of Science ®Google Scholar
• Sun, Y. F., S. B. Liu, F. L. Meng, J. Y. Liu, Z. Jin, L. T. Kong, and J. H. Liu. 2012. “Metal Oxide Nanostructures and Their Gas Sensing Properties: A Review.” Sensors (Basel, Switzerland) 12 (3): 2610–2631. doi:10.3390/s120302610.
   PubMed Web of Science ®Google Scholar
• Tan, D., D. S. Goerlitz, R. G. Dumitrescu, D. Han, F. Seillier-Moiseiwitsch, S. M. Spernak, R. A. Orden, J. Chen, R. Goldman, and P. G. Shields. 2008. “Associations between Cigarette Smoking and Mitochondrial DNA Abnormalities in Buccal Cells.” Carcinogenesis 29 (6): 1170–1177. doi:10.1093/carcin/bgn034.
   PubMed Web of Science ®Google Scholar
• Wanekaya, A. K. 2011. “Applications of Nanoscale Carbon-Based Materials in Heavy Metal Sensing and Detection.” The Analyst 136 (21): 4383–4391. doi:10.1039/c1an15574a.
   PubMed Web of Science ®Google Scholar
• Wang, X., I. Rhee, Y. Wang, and Y. Xi. 2014. “Compressive Strength, Chloride Permeability, and Freeze-Thaw Resistance of MWNT Concretes under Different Chemical Treatments.” The Scientific World Journal 2014: 572102. doi:10.1155/2014/572102.
   Google Scholar
• Wang, X., P. Katwa, R. Podila, P. Chen, P. C. Ke, A. M. Rao, D. M. Walters, C. J. Wingard, and J. M. Brown. 2011. “Multi-Walled Carbon Nanotube Instillation Impairs Pulmonary Function in C57BL/6 Mice.” Particle and Fibre Toxicology 8 (1): 24. doi:10.1186/1743-8977-8-24.
   PubMedGoogle Scholar
• Wickliffe, J. K., B. E. Rodgers, R. K. Chesser, C. J. Phillips, S. P. Gaschak, and R. J. Baker. 2003. “Mitochondrial DNA Heteroplasmy in Laboratory Mice Experimentally Enclosed in the Radioactive Chernobyl Environment.” Radiation Research 159 (4): 458–464. doi:10.1667/0033-7587(2003)159
   PubMed Web of Science ®Google Scholar
• Xia, T., R. F. Hamilton, Jr, J. C. Bonner, E. D. Crandall, A. Elder, F. Fazlollahi, T. A. Girtsman, et al. 2013. “Interlaboratory Evaluation of Cytotoxicity and Inflammatory Responses to Engineered Nanomaterials: The NIEHS Nano Go Consortium.” Environmental Health Perspectives 121 (6): 683. doi:10.1289/ehp.1306561.
   PubMed Web of Science ®Google Scholar
• Zhang, T., M. Tang, Y. Yao, Y. Ma, and Y. Pu. 2019. “MWCNT Interactions with Protein: Surface-Induced Changes in Protein Adsorption and the Impact of Protein Corona on Cellular Uptake and Cytotoxicity.” International Journal of Nanomedicine 14: 993–1009. doi:10.2147/IJN.S191689.
   PubMed Web of Science ®Google Scholar
• Zhu, S., B. Zhu, A. Huang, Y. Hu, G. Wang, and F. Ling. 2016. “Toxicological Effects of Multi-Walled Carbon Nanotubes on Saccharomyces cerevisiae: The Uptake Kinetics and Mechanisms and the Toxic Responses.” Journal of Hazardous Materials 318: 650–662. doi:10.1016/j.jhazmat.2016.07.049.
   PubMed Web of Science ®Google Scholar