Evaluation of toxicity of halloysite nanotubes and multi-walled carbon nanotubes to endothelial cells in vitro and blood vessels in vivo

References

• Anozie, U. C., and P. Dalhaimer. 2017. “Molecular Links Among Non-Biodegradable Nanoparticles, Reactive Oxygen Species, and Autophagy.” Advanced Drug Delivery Reviews 122: 65–73. doi:10.1016/j.addr.2017.01.001.
   PubMed Web of Science ®Google Scholar
• Benjamin, E. J.,   Muntner, P. Alonso, A. Bittencourt, M. S. Callaway, C. W. Carson, A. P. Chamberlain, et al. 2019. “Heart Disease and Stroke Statistics-2019 Update: A Report from the American Heart Association.” Circulation 139 (10): e56–e528. doi:10.1161/CIR.0000000000000659.
   PubMed Web of Science ®Google Scholar
• Cao, Y., and Y. Luo. 2019. “Pharmacological and Toxicological Aspects of Carbon Nanotubes (CNTs) to Vascular System: A Review.” Toxicology and Applied Pharmacology 385: 114801. doi:10.1016/j.taap.2019.114801.
   PubMed Web of Science ®Google Scholar
• Cao, Y., Y. Gong, L. Liu, Y. Zhou, X. Fang, C. Zhang, Y. Li, and J. Li. 2017. “The Use of Human Umbilical Vein Endothelial Cells (HUVECs) as an in Vitro Model to Assess the Toxicity of Nanoparticles to Endothelium: A Review.” Journal of Applied Toxicology 37 (12): 1359–1369. doi:10.1002/jat.3470.
   PubMed 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. 2014. “Vascular Effects of Multiwalled Carbon Nanotubes in Dyslipidemic ApoE-/- Mice and Cultured Endothelial Cells.” Toxicological Sciences 138 (1): 104–116. doi:10.1093/toxsci/kft328.
   PubMed Web of Science ®Google Scholar
• Cao, Y., J. Long, L. Liu, T. He, L. Jiang, C. Zhao, and Z. Li. 2017. “A Review of Endoplasmic Reticulum (ER) Stress and Nanoparticle (NP) Exposure.” Life Sciences 186: 33–42. doi:10.1016/j.lfs.2017.08.003.
   PubMed Web of Science ®Google Scholar
• Cao, Y., M. Roursgaard, P. H. Danielsen, P. Moller, and S. Loft. 2014. “Carbon Black Nanoparticles Promote Endothelial Activation and Lipid Accumulation in Macrophages Independently of Intracellular ROS Production.” PLOS One 9 (9): e106711. doi:10.1371/journal.pone.0106711.
   PubMed Web of Science ®Google Scholar
• Chang, S., X. Zhao, S. Li, T. Liao, J. Long, Z. Yu, and Y. Cao. 2018. “Cytotoxicity, Cytokine Release and ER Stress-Autophagy Gene Expression in Endothelial Cells and Alveolar-Endothelial co-Culture Exposed to Pristine and Carboxylated Multi-Walled Carbon Nanotubes.” Ecotoxicology and Environment Safety. 161: 569–577. doi:10.1016/j.ecoenv.2018.06.025.
   PubMed Web of Science ®Google Scholar
• Christophersen, D. V., N. R. Jacobsen, M. H. Andersen, S. P. Connell, K. K. Barfod, M. B. Thomsen, M. R. Miller, et al. 2016. “Cardiovascular Health Effects of Oral and Pulmonary Exposure to multi-walled carbon nanotubes in ApoE-deficient mice.” Toxicology 371: 29–40. doi:10.1016/j.tox.2016.10.003.
   PubMed Web of Science ®Google Scholar
• Davis, G., J. Lucero, C. Fellers, J. D. McDonald, and A. K. Lund. 2018. “The Effects of Subacute Inhaled Multi-Walled Carbon Nanotube Exposure on Signaling Pathways Associated with Cholesterol Transport and Inflammatory Markers in the Vasculature of Wild-Type Mice.” Toxicology Letters 296: 48–62. doi:10.1016/j.toxlet.2018.08.004.
   PubMed Web of Science ®Google Scholar
• Dong, J., and Q. Ma. 2016. “Myofibroblasts and Lung Fibrosis Induced by Carbon Nanotube Exposure.” Particle and Fibre Toxicology 13 (1): 60doi:10.1186/s12989-016-0172-2.
   PubMed Web of Science ®Google Scholar
• Fakhrullina, G. I., F. S. Akhatova, Y. M. Lvov, and R. F. Fakhrullin. 2015. “Toxicity of Halloysite Clay Nanotubes in Vivo: A Caenorhabditis elegans Study.” Environmental Science: Nano 2 (1): 54–59. doi:10.1039/C4EN00135D.
   Web of Science ®Google Scholar
• Fan, Y., H. Lu, W. Liang, W. Hu, J. Zhang, and Y. E. Chen. 2017. “Kruppel-like Factors and Vascular Wall Homeostasis.” Journal of Molecular Cell Biology 9 (5): 352–363. doi:10.1093/jmcb/mjx037.
   PubMed Web of Science ®Google Scholar
• Fizir, M., P. Dramou, N. S. Dahiru, W. Ruya, T. Huang, and H. He. 2018. “Halloysite Nanotubes in Analytical Sciences and in Drug Delivery: A Review.” Mikrochim Acta 185 (8): 389–2908. doi:10.1007/s00604-018-2908-1.
   PubMed Web of Science ®Google Scholar
• Gao, S., G. Tang, D. Hua, R. Xiong, J. Han, S. Jiang, Q. Zhang, and C. Huang. 2019. “Stimuli-Responsive Bio-Based Polymeric Systems and Their Applications.” Journal of Materials Chemistry. B 7 (5): 709–729. doi:10.1039/C8TB02491J.
   PubMed Web of Science ®Google Scholar
• Garcia, V., and W. C. Sessa. 2019. “Endothelial NOS: Perspective and Recent Developments.” British Journal of Pharmacology 176 (2): 189–196. doi:10.1111/bph.14522.
   PubMed Web of Science ®Google Scholar
• Guo, F., N. Ma, Y. Horibe, S. Kawanishi, M. Murata, and Y. Hiraku. 2012. “Nitrative DNA Damage Induced by Multi-Walled Carbon Nanotube via Endocytosis in Human Lung Epithelial Cells.” Toxicology and Applied Pharmacology 260 (2): 183–192. doi:10.1016/j.taap.2012.02.010.
   PubMed Web of Science ®Google Scholar
• Kamalieva, R. F., I. R. Ishmukhametov, S. N. Batasheva, E. V. Rozhina, and R. F. Fakhrullin. 2018. “Uptake of Halloysite Clay Nanotubes by Human Cells: Colourimetric Viability Tests and Microscopy Study.” Nano-Structures & Nano-Objects 15: 54–60. doi:10.1016/j.nanoso.2018.03.009.
   Google Scholar
• Lai, X., M. Agarwal, Y. M. Lvov, C. Pachpande, K. Varahramyan, and F. A. Witzmann. 2013. “Proteomic Profiling of Halloysite Clay Nanotube Exposure in Intestinal Cell Co-Culture.” Journal of Applied Toxicology 33 (11): 1316–1329. doi:10.1002/jat.2858.
   PubMed Web of Science ®Google Scholar
• Li, S., H. Liu, Z. Zhou, and Y. Cao. 2020. “Titanate Nanotubes at Non-Cytotoxic Concentrations Affect NO Signaling Pathway in Human Umbilical Vein Endothelial Cells.” Toxicology in Vitro : An International Journal Published in Association with BIBRA 62: 104689. doi:10.1016/j.tiv.2019.104689.
   PubMed Web of Science ®Google Scholar
• Li, X., Y. Tang, C. Chen, D. Qiu, and Y. Cao. 2019. “PEGylated Gold Nanorods Are Not Cytotoxic to Human Endothelial Cells but Affect Kruppel-like Factor Signaling pathway.” Toxicology and Applied Pharmacology 382: 114758. doi:10.1016/j.taap.2019.114758.
   PubMed Web of Science ®Google Scholar
• Li, Z., T. Liu, J. Long, Y. Wu, B. Yan, P. Ma, and Y. Cao. 2019. “The Toxicity of Hydroxylated and Carboxylated Multi-Walled Carbon Nanotubes to Human Endothelial Cells Was Not Exacerbated by ER Stress Inducer.” Chinese Chemical Letters 30 (3): 582–586. doi:10.1016/j.cclet.2018.12.011.
   Web of Science ®Google Scholar
• Li, Z., Y. Zhang, D. Zhu, S. Li, X. Yu, Y. Zhao, X. Ouyang, Z. Xie, and L. Li. 2017. “Transporting Carriers for Intracellular Targeting Delivery via non-endocytic uptake pathways .” Drug Delivery 24 (sup1): 45–55. doi:10.1080/10717544.2017.1391889.
   PubMedGoogle Scholar
• Lin, J., Y. Jiang, Y. Luo, H. Guo, C. Huang, J. Peng, and Y. Cao. 2020. “Multi-Walled Carbon Nanotubes (MWCNTs) Transformed THP-1 Macrophages into Foam Cells: Impact of Pulmonary Surfactant Component Dipalmitoylphosphatidylcholine.” Journal of Hazardous Materials 392: 122286. doi:10.1016/j.jhazmat.2020.122286.
   PubMed Web of Science ®Google Scholar
• Liu, M., R. Fakhrullin, A. Novikov, A. Panchal, and Y. Lvov. 2019. “Tubule Nanoclay-Organic Heterostructures for Biomedical Applications.” Macromolecular Bioscience 19 (4): e1800419. doi:10.1002/mabi.201800419.
   PubMed Web of Science ®Google Scholar
• Long, J., X. Li, Y. Kang, Y. Ding, Z. Gu, and Y. Cao. 2018. “Internalization, Cytotoxicity, Oxidative Stress and Inflammation of Multi-Walled Carbon Nanotubes in Human Endothelial Cells: Influence of Pre-Incubation with Bovine Serum Albumin.” RSC Advances 8 (17): 9253–9260. doi:10.1039/C8RA00445E.
   PubMed Web of Science ®Google Scholar
• Long, J., W. Ma, Z. Yu, H. Liu, and Y. Cao. 2019. “Multi-walled Carbon Nanotubes (MWCNTs) Promoted Lipid Accumulation in THP-1 Macrophages Through Modulation of Endoplasmic Reticulum (ER) Stress .” Nanotoxicology 13 (7): 938–951. doi:10.1080/17435390.2019.1597204.
   PubMed Web of Science ®Google Scholar
• Long, J., Y. Xiao, L. Liu, and Y. Cao. 2017. “The Adverse Vascular Effects of Multi-Walled Carbon Nanotubes (MWCNTs) to Human Vein Endothelial Cells (HUVECs) In Vitro: Role of Length of MWCNTs.” Journal of Nanobiotechnology 15 (1): 80. doi:10.1186/s12951-017-0318-x.
   PubMedGoogle Scholar
• Long, Z., Y. P. Wu, H. Y. Gao, Y. F. Li, R. R. He, and M. Liu. 2018. “Functionalization of Halloysite Nanotubes via Grafting of Dendrimer for Efficient Intracellular Delivery of siRNA.” Bioconjugate Chemistry 29 (8): 2606–2618. doi:10.1021/acs.bioconjchem.8b00321.
   PubMed Web of Science ®Google Scholar
• Long, Z., Y. P. Wu, H. Y. Gao, J. Zhang, X. Ou, R. R. He, and M. Liu. 2018. “In Vitro and In Vivo Toxicity Evaluation of Halloysite Nanotubes.” Journal of Materials Chemistry B 6 (44): 7204–7216. doi:10.1039/c8tb01382a.
   PubMed Web of Science ®Google Scholar
• Mohajeri, M.,. B. Behnam, and A. Sahebkar. 2018. “Biomedical Applications of Carbon Nanomaterials: Drug and Gene Delivery Potentials.” Journal of Cellular Physiology 234 (1): 298–319. doi:10.1002/jcp.26899.
   PubMed Web of Science ®Google Scholar
• Moller, P., and N. R. Jacobsen. 2017. “Weight of Evidence Analysis for Assessing the Genotoxic Potential of Carbon Nanotubes.” Critical Reviews in Toxicology. 47: 867–884.
   PubMed Web of Science ®Google Scholar
• Moller, P., D. V. Christophersen, N. R. Jacobsen, A. Skovmand, A. C. Gouveia, M. H. Andersen, A. Kermanizadeh, et al. 2016. “Atherosclerosis and Vasomotor Dysfunction in Arteries of Animals after Exposure to Combustion-Derived Particulate Matter or Nanomaterials.” Critical Reviews in Toxicology 46 (5): 437–476. doi:10.3109/10408444.2016.1149451.
   PubMed Web of Science ®Google Scholar
• Moller, P., D. V. Christophersen, D. M. Jensen, A. Kermanizadeh, M. Roursgaard, N. R. Jacobsen, J. G. Hemmingsen, et al. 2014. “Role of Oxidative Stress in Carbon Nanotube-Generated Health Effects.” Archives of Toxicology. 88: 1939–1964.
   PubMed Web of Science ®Google Scholar
• Monteiro-Riviere, N. A., R. J. Nemanich, A. O. Inman, Y. Y. Wang, and J. E. Riviere. 2005. “Multi-Walled Carbon Nanotube Interactions with Human Epidermal Keratinocytes.” Toxicology Letters 155 (3): 377–384. doi:10.1016/j.toxlet.2004.11.004.
   PubMed Web of Science ®Google Scholar
• Naumenko, E. A., I. D. Guryanov, R. Yendluri, Y. M. Lvov, and R. F. Fakhrullin. 2016. “Clay Nanotube-Biopolymer Composite Scaffolds for Tissue Engineering.” Nanoscale 8 (13): 7257–7271. doi:10.1039/c6nr00641h.
   PubMed Web of Science ®Google Scholar
• Orecna, M., S. H. De Paoli, O. Janouskova, T. Z. Tegegn, M. Filipova, J. E. Bonevich, K. Holada, and J. Simak. 2014. “Toxicity of Carboxylated Carbon Nanotubes in Endothelial Cells is Attenuated by Stimulation of the Autophagic Flux with the Release of Nanomaterial in Autophagic Vesicles.” Nanomedicine: Nanotechnology, Biology, and Medicine 10 (5): 939–948. doi:10.1016/j.nano.2014.02.001.
   PubMed Web of Science ®Google Scholar
• Panchal, A., G. Fakhrullina, R. Fakhrullin, and Y. Lvov. 2018. “Self-Assembly of Clay Nanotubes on Hair Surface for Medical and Cosmetic Formulations.” Nanoscale 10 (38): 18205–18216. doi:10.1039/c8nr05949g.
   PubMed Web of Science ®Google Scholar
• Rezaee, M., B. Behnam, M. Banach, and A. Sahebkar. 2018. “The Yin and Yang of Carbon Nanomaterials in Atherosclerosis.” Biotechnology Advances 36 (8): 2232–2247. doi:10.1016/j.biotechadv.2018.10.010.
   PubMed Web of Science ®Google Scholar
• Rong, R.,. Y. Zhang, Y. Zhang, Y. Hu, W. Yang, X. Hu, L. Wen, and Q. Zhang. 2019. “Inhibition of Inhaled Halloysite Nanotube Toxicity by Trehalose through Enhanced Autophagic Clearance of p62.” Nanotoxicology 13 (3): 354–368. doi:10.1080/17435390.2018.1549688.
   PubMed Web of Science ®Google Scholar
• Saleem, J., L. Wang, and C. Chen. 2018. “Carbon-Based Nanomaterials for Cancer Therapy via Targeting Tumor Microenvironment.” Advanced Healthcare Materials 7 (20): e1800525. doi:10.1002/adhm.201800525.
   PubMed Web of Science ®Google Scholar
• Santos, A. C., C. Ferreira, F. Veiga, A. J. Ribeiro, A. Panchal, Y. Lvov, and A. Agarwal. 2018. “Halloysite Clay Nanotubes for Life Sciences Applications: From Drug Encapsulation to Bioscaffold.” Advances in Colloid and Interface Science 257: 58–70. doi:10.1016/j.cis.2018.05.007.
   PubMed Web of Science ®Google Scholar
• Setyawati, M. I., C. Y. Tay, D. Docter, R. H. Stauber, and D. T. Leong. 2015. “Understanding and Exploiting Nanoparticles’ Intimacy with the Blood Vessel and Blood.” Chemical Society Reviews 44 (22): 8174–8199. doi:10.1039/C5CS00499C.
   PubMed Web of Science ®Google Scholar
• Shen, B., R. S. Smith, Jr., Y. T. Hsu, L. Chao, and J. Chao. 2009. “Kruppel-like Factor 4 is a Novel Mediator of Kallistatin in Inhibiting Endothelial Inflammation via Increased Endothelial Nitric-Oxide Synthase Expression.” The Journal of Biological Chemistry 284 (51): 35471–35478. doi:10.1074/jbc.M109.046813.
   PubMed Web of Science ®Google Scholar
• Smith, M., and S. Wilkinson. 2017. “ER Homeostasis and Autophagy.” Essays in Biochemistry 61 (6): 625–635. doi:10.1042/EBC20170092.
   PubMed Web of Science ®Google Scholar
• Suzuki, Y., S. Tada-Oikawa, Y. Hayashi, K. Izuoka, M. Kataoka, S. Ichikawa, W. Wu, C. Zong, G. Ichihara, and S. Ichihara. 2016. “Single- and Double-Walled Carbon Nanotubes Enhance Atherosclerogenesis by Promoting Monocyte Adhesion to Endothelial Cells and Endothelial Progenitor Cell Dysfunction.” Particle and Fibre Toxicology 13 (1): 54. doi:10.1186/s12989-016-0166-0.
   PubMedGoogle Scholar
• Teradal, N. L., and R. Jelinek. 2017. “Carbon Nanomaterials in Biological Studies and Biomedicine.” Advanced Healthcare Materials 6: 10.
   Web of Science ®Google Scholar
• Thompson, L. C., N. L. Sheehan, D. M. Walters, R. M. Lust, J. M. Brown, and C. J. Wingard. 2019. “Airway Exposure to Modified Multi-Walled Carbon Nanotubes Perturbs Cardiovascular Adenosinergic Signaling in Mice.” Cardiovascular Toxicology 19 (2): 168–177. doi:10.1007/s12012-018-9487-6.
   PubMed Web of Science ®Google Scholar
• Vergaro, V.,. E. Abdullayev, Y. M. Lvov, A. Zeitoun, R. Cingolani, R. Rinaldi, and S. Leporatti. 2010. “Cytocompatibility and Uptake of Halloysite Clay nanotubes.” Biomacromolecules 11 (3): 820–826. doi:10.1021/bm9014446.
   PubMed Web of Science ®Google Scholar
• Vergaro, V.,. Y. M. Lvov, and S. Leporatti. 2012. “Halloysite Clay Nanotubes for Resveratrol Delivery to Cancer Cells.” Macromolecular Bioscience 12 (9): 1265–1271. doi:10.1002/mabi.201200121.
   PubMed Web of Science ®Google Scholar
• Walker, V. G., Z. Li, T. Hulderman, D. Schwegler-Berry, M. L. Kashon, and P. P. Simeonova. 2009. “Potential in Vitro Effects of Carbon Nanotubes on Human Aortic Endothelial Cells.” Toxicology and Applied Pharmacology 236 (3): 319–328. doi:10.1016/j.taap.2009.02.018.
   PubMed Web of Science ®Google Scholar
• Wang, L., and C. Chen. 2016. “Pathophysiologic Mechanisms of Biomedical Nanomaterials.” Toxicology and Applied Pharmacology 299: 30–40. doi:10.1016/j.taap.2016.01.022.
   PubMed Web of Science ®Google Scholar
• Wang, M., Q. Yang, J. Long, Y. Ding, X. Zou, G. Liao, and Y. Cao. 2018. “A Comparative Study of Toxicity of TiO2, ZnO, and Ag Nanoparticles to Human Aortic Smooth-Muscle Cells.” International Journal of Nanomedicine 13: 8037–8049. doi:10.2147/IJN.S188175.
   PubMed Web of Science ®Google Scholar
• Wang, R., M. Lee, K. Kinghorn, T. Hughes, I. Chuckaree, R. Lohray, E. Chow, P. Pantano, and R. Draper. 2018. “Quantitation of Cell-Associated Carbon Nanotubes: Selective Binding and Accumulation of Carboxylated Carbon Nanotubes by Macrophages.” Nanotoxicology 12 (7): 677–698. doi:10.1080/17435390.2018.1472309.
   PubMed Web of Science ®Google Scholar
• Wang, X., J. Gong, Z. Gui, T. Hu, and X. Xu. 2018. “Halloysite Nanotubes-Induced Al Accumulation and Oxidative Damage in Liver of Mice after 30-Day Repeated Oral Administration.” Environmental Toxicology 33 (6): 623–630. doi:10.1002/tox.22543.
   PubMed Web of Science ®Google Scholar
• Wu, W.,. P. Geng, J. Zhu, J. Li, L. Zhang, W. Chen, D. Zhang, Y. Lu, and X. Xu. 2019. “KLF2 Regulates eNOS Uncoupling via Nrf2/HO-1 in Endothelial Cells under Hypoxia and Reoxygenation.” Chemico-Biological Interactions 305: 105–111. doi:10.1016/j.cbi.2019.03.010.
   PubMed Web of Science ®Google Scholar
• Xu, Y. Y., J. Yang, T. Shen, F. Zhou, Y. Xia, J. Y. Fu, J. Meng, et al. 2012. “Intravenous Administration of Multi-Walled Carbon Nanotubes Affects the Formation of Atherosclerosis in Sprague-Dawley Rats.” Journal of Occupational Health 54 (5): 361–369. doi:10.1539/joh.12-0019-OA.
   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
• Zhao, X., S. Chang, J. Long, J. Li, X. Li, and Y. Cao. 2019. “The Toxicity of Multi-Walled Carbon Nanotubes (MWCNTs) to Human Endothelial Cells: The Influence of Diameters of MWCNTs.” Food and Chemical Toxicology 126: 169–177. doi:10.1016/j.fct.2019.02.026.
   PubMed Web of Science ®Google Scholar
• Zhu, Y., X. Xian, Z. Wang, Y. Bi, Q. Chen, X. Han, D. Tang, and R. Chen. 2018. “Research Progress on the Relationship between Atherosclerosis and Inflammation.” Biomolecules 8 (3): 80. doi:10.3390/biom8030080.
   PubMed Web of Science ®Google Scholar