393
Views
22
CrossRef citations to date
0
Altmetric
Articles

Cytotoxicity and genotoxicity of MWCNT-7 and crocidolite: assessment in alveolar epithelial cells versus their coculture with monocyte-derived macrophages

, , , , , & ORCID Icon show all
Pages 479-503 | Received 03 Jan 2019, Accepted 17 Nov 2019, Published online: 12 Feb 2020

References

  • Allegri, M., D. K. Perivoliotis, M. G. Bianchi, M. Chiu, A. Pagliaro, M. A. Koklioti, A. A. Trompeta, E. Bergamaschi, O. Bussolati, and C. A. Charitidis. 2016. “Toxicity Determinants of Multi-Walled Carbon Nanotubes: The Relationship between Functionalization and Agglomeration.” Toxicology Reports 3: 230–243. doi:10.1016/j.toxrep.2016.01.011.
  • Bremnes, R. M., R. Veve, E. Gabrielson, F. R. Hirsch, A. Baron, L. Bemis, R. M. Gemmill, H. A. Drabkin, W. A. Franklin. 2002. “High-Throughput Tissue Microarray Analysis used to Evaluate Biology and Prognostic Significance of the E-Cadherin Pathway in Non-Small Cell Lung Cancer.” Journal of Clinical Oncology 20 (10): 2417–2428. doi:10.1200/JCO.2002.08.159.
  • Brown, D. M., I. A. Kinloch, U. Bangert, A. H. Windle, D. M. Walters, G. S. Walker, C. A. Scotchford, K. Donaldson, V. Stone. 2007. “An In Vitro Study of the Potential of Carbon Nanotubes and Nanofibres to Induce Inflammation Mediators and Frustrated Phagocytosis.” Carbon 45: 1743–1756. doi:10.1016/j.carbon.2007.05.011.
  • Casey, A., E. Herzog, F. M. Lyng, H. J. Byrne, G. Chambers, and M. Davoren. 2008. “Single Walled Carbon Nanotubes Induce Indirect Cytotoxicity by Medium Depletion in A549 Lung Cells.” Toxicology Letters 179 (2): 78–84. doi:10.1016/j.toxlet.2008.04.006.
  • Catalán, J., K. M. Siivola, P. Nymark, H. Lindberg, S. Suhonen, H. Järventaus, A. J. Koivisto, et al. 2016. “In Vitro and in Vivo Genotoxic Effects of Straight versus Tangled Multi-Walled Carbon Nanotubes.” Nanotoxicology 10 (6): 794–806. doi:10.3109/17435390.2015.1132345.
  • Chaffer, C. L., and R. A. Weinberg. 2011. “A Perspective on Cancer Cell Metastasis.” Science 331: 1559–1564. doi:10.1126/science.1203543.
  • Chatterjee, N., J. Yang, H.-M. Kim, E. Jo, P.-J. Kim, K. Choi, and J. Choi. 2014. “Potential Toxicity of Differential Functionalized Multiwalled Carbon Nanotubes (MWCNT) in Human Cell Line (BEAS2B) and Caenorhabditis elegans.” Journal of Toxicology and Environmental Health Part A 77 (22-24): 1399–1408. doi:10.1080/15287394.2014.951756.
  • Chen, T., H. Nie, X. Gao, J. Yang, J. Pu, Z. Chen, X. Cui, Y. Wang, H. Wang, and G. Jia. 2014. “Epithelial-Mesenchymal Transition Involved in Pulmonary Fibrosis Induced by Multi-Walled Carbon Nanotubes via TGF-Beta/Smad Signaling Pathway.” Toxicology Letters 226 (2): 150–162.
  • Cheong, H. S., I. Seth, M. C. Joiner, and J. D. Tucker. 2013. “Relationships among Micronuclei, Nucleoplasmic Bridges and Nuclear Buds within Individual Cells in the Cytokinesis-Block Micronucleus Assay.” Mutagenesis 28 (4): 433–440.
  • Chortarea, S., F. Zerimariam, H. Barosova, D. Septiadi, M. J. D. Clift, A. Petri-Fink, and B. Rothen-Rutishauser. 2019. “Profibrotic Activity of Multiwalled Carbon Nanotubes upon Prolonged Exposures in Different Human Lung Cell Types.” Applied in Vitro Toxicology 5 (1): 47.
  • El Yamani, N., A. R. Collins, E. Rundén-Pran, L. M. Fjellsbø, S. Shaposhnikov, S. Zienolddiny, and M. Dusinska. 2017. “In Vitro Genotoxicity Testing of Four Reference Metal Nanomaterials, Titanium Dioxide, Zinc Oxide, Cerium Oxide and Silver: Towards Reliable Hazard Assessment.” Mutagenesis 32 (1): 117–126. doi:10.1093/mutage/gew060.
  • Essers, J., A. F. Theil, C. Baldeyron, W. A. van Cappellen, A. B. Houtsmuller, R. Kanaar, and W. Vermeulen. 2005. “Nuclear Dynamics of PCNA in DNA Replication and Repair.” Molecular and Cellular Biology 25 (21): 9350–9359. doi:10.1128/MCB.25.21.9350-9359.2005.
  • Fenech, M. 2007. “Cytokinesis-Block Micronucleus Cytome Assay.” Nature Protocols 2 (5): 1084–1104. doi:10.1038/nprot.2007.77.
  • Fukai, E., H. Sato, M. Watanabe, D. Nakae, and Y. Totsuka. 2018. “Establishment of an in Vivo Simulating co-Culture Assay Platform for Genotoxicity of Multi-Walled Carbon Nanotubes.” Cancer Science 109 (4): 1024–1031.
  • Grosse, Y., D. Loomis, K. Z. Guyton, B. Lauby-Secretan, F. El Guissassi, V. Bouvard, L. Benbrahim-Tallaa, et al. Onograph Working Group. 2015. “ Carcinogenicity of Fluoro-Edenite, Silicon Carbide Fibres and Whiskers, and Carbon Nanotubes.” The Lancet Oncology 8 (1): 24–25.
  • Hanahan, D., and R. A. Weinberg. 2011. “Hallmarks of Cancer: The Next Generation.” Cell 144 (5): 646–674. doi:10.1016/j.cell.2011.02.013.
  • He, X., S. Young, J. E. Fernback, and Q. Ma. 2012. “Single-Walled Carbon Nanotubes Induce Fibrogenic Effect by Disturbing Mitochondrial Oxidative Stress and Activating NF-κB Signaling.” Journal of Clinical Toxicology. 5. 10.4172/2161-0495.S5-005
  • Hiraku, Y., F. Guo, N. Ma, T. Yamada, S. Wang, S. Kawanishi, and M. Murata. 2015. “Multi-Walled Carbon Nanotube Induces Nitrative DNA Damage in Human Lung Epithelial Cells via HMGB1-RAGE Interaction and Toll-like Receptor 9 Activation.” Particle and Fibre Toxicology 13 (1): 16. doi:10.1186/s12989-016-0127-7.
  • Huaux, F., V. d’Ursel de Bousies, M.-A. Parent, M. Orsi, F. Uwambayinema, R. Devosse, S. Ibouraadaten, et al. 2015. “Mesothelioma Response to Carbon Nanotubes is Associated with an Early and Selective Accumulation of Immunosuppressive Monocytic Cells.” Particle and Fibre Toxicology 13 (1): 46. doi:10.1186/s12989-016-0158-0.
  • 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.
  • IARC (International Agency for Research on Cancer). 2012. IARC monographs on the evaluation of carcinogenic risks to humans, Volume 100C. A review of human carcinogens. Part C: Arsenic, metals, fibres, and dusts. IARC Working Group on the Evaluation of Carcinogenic Risks to Humans. Lyon, France: World Health Organization.
  • Jackson, P., K. Kling, K. A. Jensen, P. A. Clausen, A. M. Madsen, H. Wallin, and U. Vogel. 2015. “Characterization of Genotoxic Response to15 Multiwalled Carbon Nanotubes with Variable Physicochemical Properties Including Surface Functionalizations in the FE1-Muta(TM) Mouse Lung Epithelial Cell Line.” Environmental and Molecular Mutagenesis 56 (2): 183–203. doi:10.1002/em.21922.
  • Jensen, K. A. 2013. Deliverable 4.1: summary report on primary physicochemical properties of manufactured nanomaterials used in Nanogenotox. https://www.anses.fr/en/content/deliverable-41-summary-report-primary-physicochemical-properties-manufactured-nanomaterials
  • Jensen, K. A., K. Yahia, E. Christiansen, N. R. Jacobsen, H. Wallin, C. Guiot, O. Spalla, and O. Witschger. 2011. Towards a Method for Detecting the Potential Genotoxicity of Nanomaterials. Final Protocol for Producing Suitable Manufactured Nanomaterial Exposure Media. Nanogenotox Report; Copenhagen.
  • Jiang, L., H. Nagai, H. Ohara, S. Hara, M. Tachibana, S. Hirano, Y. Shinohara, N. Kohyama, S. Akatsuka, and S. Toyokuni. 2008. “Characteristics and Modifying Factors of Asbestos-Induced Oxidative DNA Damage.” Cancer Science 99 (11): 2142–2151. doi:10.1111/j.1349-7006.2008.00934.x.
  • Kagan, V. E., A. A. Kapralov, C. M. St Croix, S. C. Watkins, E. R. Kisin, G. P. Kotchey, K. Balasubramanian, et al. 2014. “Lung Macrophages “Digest” Carbon Nanotubes Using a Superoxide/Peroxynitrite Oxidative Pathway.” ACS Nano 248 (6): 5610–5621.
  • Kajita, M., K. M. McClinic, and P. A. Wade. 2004. “Aberrant Expression of the Transcription Factors Snail and Slug Alters the Response to Genotoxic Stress.” Molecular and Cellular Biology 24 (17): 7559–7566.
  • Kalluri, R., and R. A. Weinberg. 2009. “The Basics of Epithelial-Mesenchymal Transition.” Journal of Clinical Investigation 119 (6): 1420–1428. doi:10.1172/JCI39104.
  • Kang, B., S. Chang, Y. Dai, D. Yu, and D. Chen. 2010. “Cell Response to Carbon Nanotubes: size-Dependent Intracellular Uptake Mechanisms and Subcellular Fate.” Small 21: 2362–2366. doi:10.1002/smll.201001260.
  • Kasai, T., Y. Umeda, M. Ohnishi, T. Mine, H. Kondo, T. Takeuchi, M. Matsumoto, and S. Fukushima. 2015. “Lung Carcinogenicity of Inhaled Multi- Walled Carbon Nanotube in Rats.” Particle and Fibre Toxicology 13 (1): 53. doi:10.1186/s12989-016-0164-2.
  • 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. doi:10.3109/17435390.2012.674571.
  • Kawata, M., D. Koinuma, T. Ogami, K. Umezawa, C. Iwata, T. Watabe, and K. Miyazono. 2012. “TGF-β-Induced Epithelial-Mesenchymal Transition of A549 Lung Adenocarcinoma Cells is Enhanced by Pro-Inflammatory Cytokines Derived from RAW 264.7 Macrophage Cells.” The Journal of Biochemistry 151 (2): 205–216. doi:10.1093/jb/mvr136.
  • Kim, J.-E., H.-T. Lim, A. Minai-Tehrani, J.-T. Kwon, J.Y. Shin, C.-G. Woo, M. Choi, et al. 2010. “Toxicity and Clearance of Intratracheally Administered Multiwalled Carbon Nanotubes from Murine Lung.” Journal of Toxicology and Environmental Health Part A 73 (21-22): 1530–1543. doi:10.1080/15287394.2010.511578.
  • Kohyama, N., Y. Shinohara, and Y. Suzuki. 1996. “Mineral Phases and Some Reexamined Characteristics of the International Union against Cancer Standard Asbestos Samples.” American Journal of Industrial Medicine 30 (5): 515–528. doi:10.1002/(SICI)1097-0274(199611)30:5<515::AID-AJIM1>3.0.CO;2-S.
  • Kostarelos, K., L. Lacerda, G. Pastorin, W. Wu, S. Wieckowski, J. Luangsivilay, S. Godefroy, et al. 2007. “Cellular Uptake of Functionalized Carbon Nanotubes is Independent of Functional Group and Cell Type.” Nature Nanotechnology 2 (2): 108–113. doi:10.1038/nnano.2006.209.
  • Kuempel, E. D., M. C. Jaurand, P. Møller, Y. Morimoto, N. Kobayashi, K. E. Pinkerton, L. M. Sargent, R. C. Vermeulen, B. Fubini, and A. B. Kane. 2017. “Evaluating the Mechanistic Evidence and Key Data Gaps in Assessing the Potential Carcinogenicity of Carbon Nanotubes and Nanofibers in Humans.” Critical Reviews in Toxicology 47 (1): 1–58.
  • Lacerda, L., G. Pastorin, D. Gathercole, J. Buddle, M. Prato, A. Bianco, and K. Kostarelos. 2007. “Intracellular Trafficking of Carbon Nanotubes by Confocal Laser Scanning Microscopy.” Advanced Materials 19 (11): 1480–1484. doi:10.1002/adma.200601412.
  • Lacerda, L., J. Russier, G. Pastorin, M. A. Herrero, E. Venturelli, H. Dumortier, K. T. Al-Jamal, M. Prato, K. Kostarelos, and A. Bianco. 2012. “Translocation Mechanisms of Chemically Functionalised Carbon Nanotubes across Plasma Membranes.” Biomaterials 33 (11): 3334–3343.
  • Lamouille, S., J. Xu, and R. Derynck. 2014. “Molecular Mechanisms of Epithelial–Mesenchymal Transition.” Nature Reviews Molecular Cell Biology 15 (3): 178–196. doi:10.1038/nrm3758.
  • Landsiedel, R., U. G. Sauer, L. Ma-Hock, J. Schnekenburger, and M. Wiemann. 2014. “Pulmonary Toxicity of Nanomaterials: A Critical Comparison of Published in Vitro Assays and in Vivo Inhalation or Instillation Studies.” Nanomedicine 9 (16): 2557–2585. doi:10.2217/nnm.14.149.
  • Lindberg, H. K., G.C.-M. Falck, R. Singh, S. Suhonen, H. Järventaus, E. Vanhala, J. Catalán, P. B. Farmer, K. M. Savolainen, and H. Norppa. 2013. “Genotoxicity of Short Single-Wall and Multi-Wall Carbon Nanotubes in Human Bronchial Epithelial and Mesothelial Cells in Vitro.” Toxicology 313 (1): 24–37. doi:10.1016/j.tox.2012.12.008.
  • Liu, G., P. Cheresh, and D. W. Kamp. 2013. “Molecular Basis of Asbestos-Induced Lung Disease.” Annual Review of Pathology: Mechanisms of Disease 24 (8): 161–187. doi:10.1146/annurev-pathol-020712-163942.
  • Louro, H., M. Pinhão, J. Santos, A. Tavares, N. Vital, and M. J. Silva. 2016. “Evaluation of the Cytotoxic and Genotoxic Effects of Benchmark Multi-Walled Carbon Nanotubes in Relation to Their Physicochemical Properties.” Toxicology Letters 262: 123–134. doi:10.1016/j.toxlet.2016.09.016.
  • Moldovan, G. L., B. Pfander, and S. Jentsch. 2007. “PCNA, the Maestro of the Replication Fork.” Cell 129 (4): 665–679. doi:10.1016/j.cell.2007.05.003.
  • Møller, P., and N.R. Jacobsen. 2017. “Weight of Evidence Analysis for Assessing the Genotoxic Potential of Carbon Nanotubes.” Critical Reviews in Toxicology 47 (10): 871–888. doi:10.1080/10408444.2017.1367755.
  • Mizutani, H., T. Okano, Y. Minegishi, K. Matsuda, J. Sudoh, K. Kitamura, R. Noro, C. Soeno, A. Yoshimura, M. Seike, A. Gemma. 2010. “HSP27 Modulates Epithelial to Mesenchymal Transition of Lung Cancer Cells in a Smad-Independent Manner.” Oncology Letters 6: 1011–1016. doi:10.3892/ol.2010.190.
  • Mossman, B. T., M. Lippmann, T. W. Hesterberg, K. T. Kelsey, A. Barchowsky, and J. C. Bonner. 2011. “Pulmonary Endpoints (Lung Carcinomas and Asbestosis) following Inhalation Exposure to Asbestos.” Journal of Toxicology and Environmental Health – Part B: Critical Reviews 14 (1-4): 76–121. doi:10.1080/10937404.2011.556047.
  • Muller, J., I. Decordier, P. H. Hoet, N. Lombaert, L. Thomassen, F. Huaux, D. Lison, and M. Kirsch-Volders. 2008. “Clastogenic and Aneugenic Effects of Multi-Wall Carbon Nanotubes in Epithelial Cells.” Carcinogenesis 29 (2): 427–433. doi:10.1093/carcin/bgm243.
  • Murphy, F. A., A. Schinwald, C. A. Poland, and K. Donaldson. 2012. “The Mechanism of Pleural Inflammation by Long Carbon Nanotubes: Interaction of Long Fibres with Macrophages Stimulates Them to Amplify pro-Inflammatory Responses in Mesothelial Cells.” Particle and Fibre Toxicology 9 (1): 8. doi:10.1186/1743-8977-9-8.
  • Nagai, H., Y. Okazaki, S. 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 108 (49): E1330–8. doi:10.1073/pnas.1110013108.
  • NIOSH. 2013. Current Intelligence Bulletin 65: Occupational Exposure to Carbon Nanotubes and Nanofibers. http://www.cdc.gov/niosh/docs/2013-145/pdfs/2013-145.pdf
  • Oberdörster, G., A. Maynard, K. Donaldson, V. Castranova, J. Fitzpatrick, K. Ausman, J. Carter, et al. 2005a. “Principles for Characterizing the Potential Human Health Effects from Exposure to Nanomaterials: Elements of a Screening Strategy.” Particle and Fibre Toxicology 2 (1): 8.
  • Oberdörster, G., E. Oberdörster, and J. Oberdörster. 2005b. “Nanotoxicology: An Emerging Discipline Evolving from Studies of Ultrafine Particles.” Environmental Health Perspectives 113 (7): 823–839. doi:10.1289/ehp.7339.
  • OECD. 2010. Test No. 487: In Vitro Mammalian Cell Micronucleus Test. Paris: OECD Publishing.
  • Padmore, T., C. Stark, L. A. Turkevich, J. A. Champion. 2017. “Quantitative Analysis of the Role of Fiber Length on Phagocytosis and Inflammatory Response by Alveolar Macrophages.” Biochimica Biophysica Acta 1861 (2): 58–67. doi:10.1016/j.bbagen.2016.09.031.
  • Park, E. K., H. S. Jung, H. I. Yang, M. C. Yoo, C. Kim, and K. S. Kim. 2007. “Optimized THP-1 Differentiation is Required for the Detection of Responses to Weak Stimuli.” Inflammation Research 56 (1): 45–50. doi:10.1007/s00011-007-6115-5.
  • Pinkerton, K. E., R. P. Geh, J. D. Crapo. 1992. Treatise on Pulmonary Toxicology. Vol 1. Comparative Biology of the Normal Lung. Boca Raton, FL: CRC Press.
  • 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. doi:10.1186/s12989-016-0138-4.
  • Polyak, K., and R. A. Weinberg. 2009. “Transitions between Epithelial and Mesenchymal States: Acquisition of Malignant and Stem Cell Traits.” Nature Reviews Cancer 9 (4): 265–273. doi:10.1038/nrc2620.
  • Porter, D. W., A. F. Hubbs, R. R. Mercer, N. Wu, M. G. Wolfarth, K. Sriram, S. Leonard, L. Battelli, D. Schwegler-Berry, and S. Friend. 2010. “Mouse Pulmonary Dose- and Time Course-Responses Induced by Exposure to Multi-Walled Carbon Nanotubes.” Toxicology 269 (2-3): 136–147. doi:10.1016/j.tox.2009.10.017.
  • Poulsen, S. S., P. Jackson, K. Kling, K. B. Knudsen, V. Skaug, Z. O. Kyjovska, B. L. Thomsen, et al. 2016. “Multi-Walled Carbon Nanotube Physicochemical Properties Predict Pulmonary Inflammation and Genotoxicity.” Nanotoxicology 10 (9): 1263–1275. doi:10.1080/17435390.2016.1202351.
  • Poulsen, S., N. R. Jacobsen, S. Labib, D. Wu, M. Husain, and A. Williams. 2013. “Transcriptomic Analysis Reveals Novel Mechanistic Insight into Murine Biological Responses to Multi-Walled Carbon Nanotubes in Lungs and Cultured Lung Epithelial Cells.” PLoS One 8 (11): e80452. doi:10.1371/journal.pone.0080452.
  • Pulskamp, K., S. Diabaté, and H. F. Krug. 2007. “Carbon Nanotubes Show No Sign of Acute Toxicity but Induce Intracellular Reactive Oxygen Species in Dependence on Contaminants.” Toxicology Letters 68 (1): 58–74. doi:10.1016/j.toxlet.2006.11.001.
  • Qi, F., G. Okimoto, S. Jube, A. Napolitano, H. I. Pass, R. Laczko, R. M. Demay, et al. 2013. “Continuous Exposure to Chrysotile Asbestos Can Cause Transformation of Human Mesothelial Cells via HMGB1 and TNF-α Signaling.” The American Journal of Pathology 183 (5): 1654–1666. doi:10.1016/j.ajpath.2013.07.029.
  • Rahman, L., N. R. Jacobsen, S. A. Aziz, W. Dongmei, A. Williams, C. L. Yauk, P. White, H. Wallin, U. Vogel, and S. Halappanavar. 2017. “Multi-Walled Carbon Nanotube-Induced Genotoxic, Inflammatory and Pro-Fibrotic Responses in Mice: Investigating the Mechanisms of Pulmonary Carcinogenesis.” Mutation Research/Genetic Toxicology and Environmental Mutagenesis 823: 28–44. doi:10.1016/j.mrgentox.2017.08.005.
  • Rendal, R. E. G. 1970. “The Data Sheets on the Chemical and Physical Properties of the UICC Standard Reference Samples.” In Pneumoconiosis Proceedings of the International Conference, 1969, edited by Shapiro, H. A., 23–27. Johanesburgh, Oxford: Oxford University Press.
  • Rittinghausen, S., A. Hackbarth, O. Creutzenberg, H. Ernst, U. Heinrich, A. Leonhardt, and D. Schaudien. 2014. “The Carcinogenic Effect of Various Multi-Walled Carbon Nanotubes (MWCNTs) after Intraperitoneal Injection in Rats.” Particle and Fibre Toxicology 11 (1): 59–77. doi:10.1186/s12989-014-0059-z.
  • Rodriguez-Fernandez, L., R. Valiente, J. Gonzalez, J. C. Villegas, and M. L. Fanarraga. 2012. “Multiwalled Carbon Nanotubes Display Microtubule Biomimetic Properties in Vivo, Enhancing Microtubule Assembly and Stabilization.” ACS Nano 6 (8): 6614–6625. doi:10.1021/nn302222m.
  • Rubio, L., N. El Yamani, A. Kazimirova, M. Dusinska, and R. Marcos. 2016. “Multi-Walled Carbon Nanotubes (NM401) Induce ROS-Mediated HPRT Mutations in Chinese Hamster Lung Fibroblasts.” Environmental Research 46: 185–190. doi:10.1016/j.envres.2016.01.004.
  • Sakamoto, Y., D. Nakae, N. Fukumori, K. Tayama, A. Maekawa, K. Imai, A. Hirose, T. Nishimura, N. Ohashi, and A. Ogata. 2009. “Induction of Mesothelioma by a Single Intrascrotal Administration of Multi-Wall Carbon Nanotube in Intact Male Fischer 344 Rats.” The Journal of Toxicological Sciences 34 (1): 65–76. doi:10.2131/jts.34.65.
  • Sargent, L. M., A. F. Hubbs, S.-H. Young, M. L. Kashon, C. Z. Dinu, J. L. Salisbury, S. A. Benkovic, et al. 2012. “Single-Walled Carbon Nanotube-Induced Mitotic Disruption.” Mutation Research/Genetic Toxicology and Environmental Mutagenesis 745 (1-2): 28–37. doi:10.1016/j.mrgentox.2011.11.017.
  • Sasaki, T., M. Asakura, C. Ishioka, T. Kasai, T. Katagiri, and S. Fukushima. 2016. “In Vitro Chromosomal Aberrations Induced by Various Shapes of Multi-Walled Carbon Nanotubes (MWCNTs).” Journal of Occupational Health 58 (6): 622–631. doi:10.1539/joh.16-0099-OA.
  • Shamir, E. R., and A. J. Ewald. 2014. “Three-Dimensional Organotypic Culture: Experimental Models of Mammalian Biology and Disease.” Nature Reviews Molecular Cell Biology 10: 647–664. doi:10.1038/nrm3873.
  • 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): L698–708. doi:10.1152/ajplung.00084.2005.
  • Shvedova, A. A., A. Pietroiusti, B. Fadeel, and V. E. Kagan. 2012. “Mechanisms of Carbon Nanotube-Induced Toxicity: Focus on Oxidative Stress.” Toxicology and Applied Pharmacology 261 (2): 121–133.
  • 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): 6–21. doi:10.1186/1743-8977-11-6.
  • 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.
  • Snyder-Talkington, B. N., C. Dong, X. Zhao, J. Dymacek, D. W. Porter, M. G. Wolfarth, V. Castranova, Y. Qian, and N. L. Guo. 2015. “Multi-Walled Carbon Nanotube-Induced Gene Expression in Vitro: Concordance with in Vivo Studies.” Toxicology 328: 66–74. doi:10.1016/j.tox.2014.12.012.
  • Snyder-Talkington, B. N., Y. Qian, V. Castranova, and N. L. Guo. 2012. “New Perspectives for in Vitro Risk Assessment of Multiwalled Carbon Nanotubes: Application of Coculture and Bioinformatics.” Journal of Toxicology and Environmental Health. Part B, Critical Reviews 15 (7): 468–492. doi:10.1080/10937404.2012.736856.
  • Song, J. 2007. “EMT or Apoptosis: A Decision for TGF-Beta.” Cell Research 17 (4): 289–290. doi:10.1038/cr.2007.25.
  • Srivastava, R. K., M. Lohani, A. B. Pant, and Q. Rahman. 2009. “Cyto-Genotoxicity of Amphibole Asbestos Fibers in Cultured Human Lung Epithelial Cell Line: Role of Surface Iron.” Toxicology and Industrial Health 0 (0): 1–8.
  • Srivastava, R. K., A. B. Pant, M. P. Kashyap, V. Kumar, M. Lohani, L. Jonas, and Q. Rahman. 2011. “Multi-Walled Carbon Nanotubes Induce Oxidative Stress and Apoptosis in Human Lung Cancer Cell line-A549.” Nanotoxicology 5 (2): 195–207.
  • Suzui, M., M. Futakuchi, K. Fukamachi, T. Numano, M. Abdelgied, S. Takahashi, M. Ohnishi, et al. 2016. “Multiwalled Carbon Nanotubes Intratracheally Instilled into the Rat Lung Induce Development of Pleural Malignant Mesothelioma and Lung Tumors.” Cancer Science 107 (7): 924–935. doi:10.1111/cas.12954.
  • Tabei, Y., H. Fukui, A. Nishioka, Y. Hagiwara, K. Sato, T. Yoneda, T. Koyama, and M. Horie. 2019. “Effect of Iron Overload from Multi Walled Carbon Nanotubes on Neutrophil-like Differentiated HL-60 Cells.” Scientific Reports 9 (1): 2045–2322.
  • Takagi, A., A. Hirose, M. Futakuchi, H. Tsuda, and J. Kanno. 2012. “Dose-Dependent Mesothelioma Induction by Intraperitoneal Administration of Multi-Wall Carbon Nanotubes in p53 Heterozygous Mice.” Cancer Science 103 (8): 1440–1444.
  • Takagi, A., A. Hirose, T. Nishimura, N. Fukumori, A. Ogata, N. Ohashi, S. Kitajima, and J. Kanno. 2008. “Induction of Mesothelioma in p53 + / − Mouse by Intraperitoneal Application of Multi-Wall Carbon Nanotube.” The Journal of Toxicological Sciences 33 (1): 105–116. doi:10.2131/jts.33.105.
  • Tavares, A. M., H. Louro, S. Antunes, S. Quarré, S. Simar, P.-J. De Temmerman, E. Verleysen, et al. 2014. “Genotoxicity Evaluation of Nanosized Titanium Dioxide, Synthetic Amorphous Silica and Multi-Walled Carbon Nanotubes in Human Lymphocytes.” Toxicology in Vitro 28 (1): 60–69. doi:10.1016/j.tiv.2013.06.009.
  • Taylor, A. J., C. D. Mcclure, K. A. Shipkowski, E. A. Thompson, S. Hussain, S. Garantziotis, G. N. Parsons, and J. C. Bonner. 2014. “Atomic Layer Deposition Coating of Carbon Nanotubes with Aluminum Oxide Alters Pro-Fibrogenic Cytokine Expression by Human Mononuclear Phagocytes in Vitro and Reduces Lung Fibrosis in Mice in Vivo.” PLoS One 9 (9): e106870. doi:10.1371/journal.pone.0106870.
  • Thomas, P., and M. Fenech. 2011. “Cytokinesis-Block Micronucleus Cytome Assay in Lymphocytes.” Methods in Molecular Biology 682: 217–234.
  • Thomas, P., K. Umegaki, and M. Fenech. 2003. “Nucleoplasmic Bridges Are a Sensitive Measure of Chromosome Rearrangement in the Cytokinesis-Block Micronucleus Assay.” Mutagenesis 18 (2): 187–194. doi:10.1093/mutage/18.2.187.
  • Timbrell, V. 1970. “Characteristics of the International Union against Cancer Standard Reference Samples of Asbestos.” In Shapiro, H. A. (ed.). Pneumoconiosis Proceedings of the International Conference, 1969, Johanesburgh, Oxford: Oxford University Press, pp 28–36
  • Timbrell, V., and R. E. G. Rendall. 1972. “Preparation of the UICC Standard Reference Samples of Asbestos.” Powder Technology 5 (5): 279–287. doi:10.1016/0032-5910(72)80032-9.
  • Tretyakova, N. Y., J. S. Wishnok, and S. R. Tannenbaum. 2000. “Peroxynitrite-Induced Secondary Oxidative Lesions at Guanine Nucleobases: Chemical Stability and Recognition by the Fpg DNA Repair Enzyme.” Chemical Research in Toxicology 13 (7): 658–664. doi:10.1021/tx000083x.
  • Vales, G., L. Rubio, and R. Marcos. 2016. “Genotoxic and Cell-Transformation Effects of Multi-Walled Carbon Nanotubes (MWCNT) following in Vitro Sub-Chronic Exposures.” Journal of Hazardous Materials 306: 193–202. doi:10.1016/j.jhazmat.2015.12.021.
  • Ventura, C., A. F. Lourenço, A. Sousa-Uva, P. J. T. Ferreira, and M. J. Silva. 2018. “Evaluating the Genotoxicity of Cellulose Nanofibrils in a co-Culture of Human Lung Epithelial Cells and Monocyte-Derived Macrophages.” Toxicology Letters 291: 173–183.
  • Vietti, G., D. Lison, and S. van den Brule. 2015. “Mechanisms of Lung Fibrosis Induced by Carbon Nanotubes: Towards an Adverse Outcome Pathway (AOP).” Part Fibre Toxicol 13 (1): 11.
  • Visalli, G., Bertuccio, M. P., Iannazzo, D., Piperno, A., Pistone, A., and Pietro Di, A. 2015. “Toxicological Assessment of Multi-Walled Carbon Nanotubes on A549 Human Lung Epithelial Cells.” Toxicol in Vitro 29 (2): 352–362.
  • Visalli, G., A. Facciolà, M. Currò, P. Laganà, V. La Fauci, D. Iannazzo, A. Pistone, and A. Di Pietro. 2019. “Mitochondrial Impairment Induced by Sub-Chronic Exposure to Multi-Walled Carbon Nanotubes.” International Journal of Environmental Research and Public Health 16 (5): 792.
  • Visalli, G., A. Facciolà, D. Iannazzo, A. Piperno, A. Pistone, and A. Di Pietro. 2017. “The Role of the Iron Catalyst in the Toxicity of Multi-Walled Carbon Nanotubes (MWCNTs).” Journal of Trace Elements in Medicine and Biology 43: 153–160.
  • Wang, P., X. Nie, Y. Wang, Y. Li, C. Ge, L. Zhang, L. Wang, et al. 2013. “Multiwall Carbon Nanotubes Mediate Macrophage Activation and Promote Pulmonary Fibrosis through TGF-β/Smad Signaling Pathway.” Small 9 (22): 3799–3811.
  • Wang, P., Y. Wang, X. Nie, C. Braïni, R. Bai, and C. Chen. 2015. “Multiwall Carbon Nanotubes Directly Promote Fibroblast-Myofibroblast and Epithelial-Mesenchymal Transitions through the Activation of the TGF-β/Smad Signaling Pathway.” Small 11 (4): 446–455. doi:10.1002/smll.201303588.
  • Yasui, M., N. Kamoshita, T. Nishimura, and M. Honma. 2015. “Mechanism of Induction of Binucleated Cells by Multiwalled Carbon Nanotubes as Revealed by Live-Cell Imaging Analysis.” Genes and Environment: The Official Journal of the Japanese Environmental Mutagen Society 37: 6doi:10.1186/s41021-015-0003-y.
  • Ye, S. F., Y. H. Wu, Z. Q. Hou, and Q. Q. Zhang. 2009. “ROS and NF-kappaB Are Involved in Upregulation of IL-8 in A549 Cells Exposed to Multi-Walled Carbon Nanotubes.” Biochemical and Biophysical Research Communications 379 (2): 643–648. doi:10.1016/j.bbrc.2008.12.137.
  • Yu, M., R. Chen, Z. Jia, J. Chen, J. Lou, S. Tang, and X. Zhang. 2016. “MWCNTs Induce ROS Generation, ERK Phosphorylation, and SOD-2 Expression in Human Mesothelial Cells.” International Journal of Toxicology 35 (1): 17–26. doi:10.1177/1091581815591223.
  • Yu, K.-N., J. E. Kim, H. W. Seo, C. Chae, and M.-H. Cho. 2013. “Differential Toxic Responses between Pristine and Functionalized Multiwall Nanotubes Involve Induction of Autophagy Accumulation in Murine Lung.” Journal of Toxicology and Environmental Health Part A 76 (23): 1282–1292. doi:10.1080/15287394.2013.850137.
  • Zhang, Y., and B. Yan. 2012. “Cell Cycle Regulation by Carboxylated Multiwalled Carbon Nanotubes through p53-Independent Induction of p21 under the Control of the BMP Signaling Pathway.” Chemical Research in Toxicology 25 (6): 1212–1221.
  • Zhou, L., H. J. Forman, Y. Ge, and J. Lunec. 2017. “Multi-Walled Carbon Nanotubes: A Cytotoxicity Study in Relation to Functionalization, Dose and Dispersion.” Toxicology in Vitro 42: 292–298.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.