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Articles

Inhibition of inhaled halloysite nanotube toxicity by trehalose through enhanced autophagic clearance of p62

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Pages 354-368 | Received 20 Jun 2018, Accepted 14 Nov 2018, Published online: 01 Feb 2019

References

  • Aguib, Y., A. Heiseke, S. Gilch, C. Riemer, M. Baier, A. Ertmer, and H. M. Schätzl. 2009. “Autophagy Induction by Trehalose Counter-Acts Cellular Prion-Infection.” Autophagy 5 (3): 361–369.
  • Baisch, B. L., N. M. Corson, P. Wade-Mercer, R. Gelein, A. J. Kennell, G. Oberdörster, and A. Elder. 2014. “Equivalent Titanium Dioxide Nanoparticle Deposition by Intratracheal Instillation and Whole Body Inhalation: The Effect of Dose Rate on Acute Respiratory Tract Inflammation.” Particle and Fibre Toxicology 11 (1): 5.
  • Bjørkøy, G., T. Lamark, A. Brech, H. Outzen, M. Perander, A. Øvervatn, H. Stenmark., et al. 2005. “P62/Sqstm1 Forms Protein Aggregates Degraded by Autophagy and Has a Protective Effect on Huntingtin-Induced Cell Death.” The Journal of Cell Biology 171 (4): 603–614.
  • Brook, R. D., S. Rajagopalan, C. A. Pope, J. R. Brook, A. Bhatnagar, A. V. Diez-Roux, F. Holguin., et al. 2010. “Particulate Matter Air Pollution and Cardiovascular disease: An update to the scientific statement from the American Heart Association.” Circulation 121 (21): 2331–2378.
  • Castillo, K., M. Nassif, V. Valenzuela, F. Rojas, S. Matus, G. Mercado, F. A. Court., et al. 2013. “Trehalose Delays the Progression of Amyotrophic Lateral Sclerosis by Enhancing Autophagy in Motoneurons.” Autophagy 9 (9): 1308–1320.
  • Cavallaro, G., G. Lazzara, L. Lisuzzo, S. Milioto, and F. Parisi. 2018. “Selective Adsorption of Oppositely Charged Pnipaam on Halloysite Surfaces: A Route to Thermo-Responsive Nanocarriers.” Nanotechnology 29 (32): 325702.
  • Cavallaro, G., G. Lazzara, S. Milioto, F. Parisi, V. Evtugyn, E. Rozhina, and R. Fakhrullin. 2018. “Nanohydrogel Formation within the Halloysite Lumen for Triggered and Sustained Release.” ACS Applied Materials and Interfaces 10 (9): 8265–8273.
  • Collins, J., C. Robinson, H. Danhof, C. Knetsch, H. van Leeuwen, T. Lawley, J. Auchtung., et al. 2018. “Dietary Trehalose Enhances Virulence of Epidemic Clostridium Difficile.” Nature 553 (7688): 291.
  • Davis, J. M. 1993. In Vivo Assays to Evaluate the Pathogenic Effects of Minerals in Rodents. Washington, DC (United States); Mineralogical Society of America
  • Donaldson, K., and A. Seaton. 2012. “A Short History of the Toxicology of Inhaled Particles.” Particle and Fibre Toxicology 9 (1): 13.
  • Dong, L., Y. Liu, Y. Lu, L. Zhang, N. Man, L. Cao, K. Ma., et al. 2013. “Tuning Magnetic Property and Autophagic Response for Self‐Assembled Ni–Co Alloy Nanocrystals.” Advanced Functional Materials 23 (47): 5930–5940.
  • Driscoll, K. E., D. L. Costa, G. Hatch, R. Henderson, G. Oberdorster, H. Salem, and R. B. Schlesinger. 2000. “Intratracheal Instillation as an Exposure Technique for the Evaluation of Respiratory Tract Toxicity: Uses and Limitations.” Toxicological Sciences 55 (1): 24–35.
  • Fakhrullin, R. F., and Y. M. Lvov. 2016. “Halloysite Clay Nanotubes for Tissue Engineering.” Nanomedicine 11 (17): 2243–2246.
  • 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.
  • Grassian, V. H., P. T. O’Shaughnessy, A. Adamcakova-Dodd, J. M. Pettibone, and P. S. Thorne. 2007. “Inhalation Exposure Study of Titanium Dioxide Nanoparticles with a Primary Particle Size of 2 to 5 Nm.” Environmental Health Perspectives 115 (3): 397–402.
  • Harris, J. 2011. “Autophagy and Cytokines.” Cytokine 56 (2): 140–144.
  • Janku, F., D. J. McConkey, D. S. Hong, and R. Kurzrock. 2011. “Autophagy as a Target for Anticancer Therapy.” Nature Reviews Clinical Oncology 8 (9): 528–539.
  • Kassianov, E., J. Barnard, M. Pekour, L. K. Berg, J. Shilling, C. Flynn, F. Mei., et al. 2014. “Simultaneous Retrieval of Effective Refractive Index and Density from Size Distribution and Light-Scattering Data: Weakly Absorbing Aerosol.” Atmospheric Measurement Techniques 7 (10): 3247–3261.
  • Klionsky, D. J., K. Abdelmohsen, A. Abe, M. J. Abedin, H. Abeliovich, A. Acevedo Arozena, H. Adachi., et al. 2016. “Guidelines for the Use and Interpretation of Assays for Monitoring autophagy (3rd edition).” Autophagy 12 (1): 1–222.
  • Kolosnjaj-Tabi, J., L. Lartigue, Y. Javed, N. Luciani, T. Pellegrino, C. Wilhelm, D. Alloyeau., et al. 2016. “Biotransformations of Magnetic Nanoparticles in the Body.” Nano Today 11 (3): 280–284.
  • Kryuchkova, M., A. Danilushkina, Y. Lvov, and R. Fakhrullin. 2016. “Evaluation of Toxicity of Nanoclays and Graphene Oxide in Vivo: A Paramecium Caudatum Study.” Environmental Science: Nano 3 (2): 442–452.
  • Lazzara, G., G. Cavallaro, A. Panchal, R. Fakhrullin, A. Stavitskaya, V. Vinokurov, and Y. Lvov. 2018. “An Assembly of Organic-Inorganic Composites Using Halloysite Clay Nanotubes.” Current Opinion in Colloid and Interface Science 35: 42–50.
  • Lee, H.-M., D.-M. Shin, J.-M. Yuk, G. Shi, D.-K. Choi, S.-H. Lee, S. M. Huang., et al. 2011. “Autophagy Negatively Regulates Keratinocyte Inflammatory Responses via Scaffolding Protein P62/Sqstm1.” Journal of Immunology 186 (2): 1248–58.
  • Lelieveld, J., J. Evans, M. Fnais, D. Giannadaki, and A. Pozzer. 2015. “The Contribution of Outdoor Air Pollution Sources to Premature Mortality on a Global Scale.” Nature 525 (7569): 367–371.
  • Leong, B., J. Coombs, C. Sabaitis, D. Rop, and C. Aaron. 1998. “Quantitative Morphometric Analysis of Pulmonary Deposition of Aerosol Particles Inhaled via Intratracheal Nebulization, Intratracheal Instillation or Nose‐Only Inhalation in Rats.” Journal of Applied Toxicology 18 (2): 149–160.
  • Levine, B. 2007. “Cell Biology: Autophagy and Cancer.” Nature 446 (7137): 745–747.
  • Levine, B., and D. J. Klionsky. 2004. “Development by Self-Digestion: Molecular Mechanisms and Biological Functions of Autophagy.” Developmental Cell 6 (4): 463–477.
  • Levine, B., N. Mizushima, and H. W. Virgin. 2011. “Autophagy in Immunity and Inflammation.” Nature 469 (7330): 323.
  • Li, C., H. Liu, Y. Sun, H. Wang, F. Guo, S. Rao, J. Deng., et al. 2009. “Pamam Nanoparticles Promote Acute Lung Injury by Inducing Autophagic Cell Death through the Akt-Tsc2-Mtor Signaling Pathway.” Journal of Molecular Cell Biology 1 (1): 37–45.
  • Liu, M., Z. Jia, D. Jia, and C. Zhou. 2014. “Recent Advance in Research on Halloysite Nanotubes-Polymer Nanocomposite.” Progress in Polymer Science 39 (8): 1498–1525.
  • Liu, H., Y. Zhang, N. Yang, Y. Zhang, X. Liu, C. Li, Y. Zhao., et al. 2011. “A Functionalized Single-Walled Carbon Nanotube-Induced Autophagic Cell Death in Human Lung Cells through Akt–Tsc2-Mtor Signaling.” Cell Death and Disease 2 (5): e159.
  • 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: 7204–7216.
  • Lvov, Y., and E. Abdullayev. 2013. “Functional Polymer–Clay Nanotube Composites with Sustained Release of Chemical Agents.” Progress in Polymer Science 38 (10–11): 1690–1719.
  • Lvov, Y. M., M. M. DeVilliers, and R. F. Fakhrullin. 2016. “The Application of Halloysite Tubule Nanoclay in Drug Delivery.” Expert Opinion on Drug Delivery 13 (7): 977–986.
  • Lvov, Y., W. Wang, L. Zhang, and R. Fakhrullin. 2016. “Halloysite Clay Nanotubes for Loading and Sustained Release of Functional Compounds.” Advanced Materials 28 (6): 1227–1250.
  • Ma, X., Y. Wu, S. Jin, Y. Tian, X. Zhang, Y. Zhao, L. Yu., et al. 2011. “Gold Nanoparticles Induce Autophagosome Accumulation through Size-Dependent Nanoparticle Uptake and Lysosome Impairment.” ACS na 5 (11): 8629–8639.
  • Makaremi, M., P. Pasbakhsh, G. Cavallaro, G. Lazzara, Y. K. Aw, S. M. Lee, and S. Milioto. 2017. “Effect of Morphology and Size of Halloysite Nanotubes on Functional Pectin Bionanocomposites for Food Packaging Applications.” ACS Applied Materials and Interfaces 9 (20): 17476–17488.
  • Medzhitov, R. 2008. “Origin and Physiological Roles of Inflammation.” Nature 454 (7203): 428.
  • Miller, F. J. 2000. “Dosimetry of Particles in Laboratory Animals and Humans in Relationship to Issues Surrounding Lung Overload and Human Health Risk Assessment: A Critical Review.” Inhalation Toxicology 12 (1): 19–57.
  • Miller, M. R., J. B. Raftis, J. P. Langrish, S. G. McLean, P. Samutrtai, S. P. Connell, S. Wilson., et al. 2017. “Inhaled Nanoparticles Accumulate at Sites of Vascular Disease.” ACS na 11 (5): 4542–4552.
  • Mizushima, N., B. Levine, A. M. Cuervo, and D. J. Klionsky. 2008. “Autophagy Fights Disease through Cellular Self-Digestion.” Nature 451 (7182): 1069.
  • Möhler, O., S. Benz, H. Saathoff, M. Schnaiter, R. Wagner, J. Schneider, S. Walter., et al. 2008. “The Effect of Organic Coating on the Heterogeneous Ice Nucleation Efficiency of Mineral Dust Aerosols.” Environmental Research Letters 3 (2): 025007.
  • 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.
  • Nel, A., T. Xia, L. Mädler, and N. Li. 2006. “Toxic Potential of Materials at the Nanolevel.” Science (New York, N.Y.) 311 (5761): 622–627.
  • Otterbein, L. E., F. H. Bach, J. Alam, M. Soares, H. T. Lu, M. Wysk, R. J. Davis., et al. 2000. “Carbon Monoxide Has anti-Inflammatory Effects Involving the Mitogen-Activated Protein Kinase Pathway.” Nature Medicine 6 (4): 422.
  • Pan, Y., S. Neuss, A. Leifert, M. Fischler, F. Wen, U. Simon, G. Schmid., et al. 2007. “ Size-dependent cytotoxicity of gold nanoparticles .” Small (Weinheim an Der Bergstrasse, Germany) 3 (11): 1941–1949.
  • Park, M. V., A. M. Neigh, J. P. Vermeulen, L. J. de la Fonteyne, H. W. Verharen, J. J. Briedé, H. van Loveren., et al. 2011. “The Effect of Particle Size on the Cytotoxicity, Inflammation, Developmental Toxicity and Genotoxicity of Silver Nanoparticles.” Biomaterials 32 (36): 9810–9817.
  • Popper, H., and F. Schaffner. 1957. Liver: Structure and Function. London: McGraw-Hill.
  • Pou, K. M., J. M. Massaro, U. Hoffmann, R. S. Vasan, P. Maurovich-Horvat, M. G. Larson, J. F. Keaney., et al. 2007. “Visceral and Subcutaneous Adipose Tissue Volumes Are Cross-Sectionally Related to Markers of Inflammation and Oxidative Stress.” Circulation 116 (11): 1234–1241.
  • Powis, G., R. Bonjouklian, M. M. Berggren, A. Gallegos, R. Abraham, C. Ashendel, L. Zalkow., et al. 1994. “Wortmannin, a Potent and Selective Inhibitor of Phosphatidylinositol-3-Kinase.” Cancer Research 54 (9): 2419–2423.
  • Rahman, I., and W. MacNee. 2000. “Oxidative Stress and Regulation of Glutathione in Lung Inflammation.” The European Respiratory Journal 16 (3): 534–554.
  • Reuter, S., S. C. Gupta, M. M. Chaturvedi, and B. B. Aggarwal. 2010. “Oxidative Stress, Inflammation, and Cancer: How Are They Linked?” Free Radical Biology and Medicine 49 (11): 1603–1616.
  • Riela, S., and R. F. Fakhrullin. 2017. “Clay-Based Drug-Delivery Systems: What Does the Future Hold?” Therapeutic Delivery 8 (8): 633–646.
  • Rong, R., X. Xu, S. Zhu, B. Li, X. Wang, and K. Tang. 2016. “Facile Preparation of Homogeneous and Length Controllable Halloysite Nanotubes by Ultrasonic Scission and Uniform Viscosity Centrifugation.” Chemical Engineering Journal 291: 20–29.
  • Ryman-Rasmussen, J. P., M. F. Cesta, A. R. Brody, J. K. Shipley-Phillips, J. I. Everitt, E. W. Tewksbury, O. R. Moss., et al. 2009. “Inhaled Carbon Nanotubes Reach the Subpleural Tissue in Mice.” Nature Nanotechnology 4 (11): 747–751.
  • Shvedova, A. A., E. Kisin, A. R. Murray, V. J. Johnson, O. Gorelik, S. Arepalli, A. F. Hubbs., et al. 2008. “Inhalation Vs. Aspiration of Single-Walled Carbon Nanotubes in C57bl/6 Mice: Inflammation, Fibrosis, Oxidative Stress, and Mutagenesis.” American Journal of Physiology. Lung Cellular and Molecular Physiology 295 (4): L552–L565.
  • Stern, S. T., P. P. Adiseshaiah, and R. M. Crist. 2012. “Autophagy and Lysosomal Dysfunction as Emerging Mechanisms of Nanomaterial Toxicity.” Particle and Fibre Toxicology 9 (1): 20.
  • Tal, M. C., M. Sasai, H. K. Lee, B. Yordy, G. S. Shadel, and A. Iwasaki. 2009. “Absence of Autophagy Results in Reactive Oxygen Species-Dependent Amplification of Rlr Signaling.” Proceedings of the National Academy of Sciences 106 (8): 2770–2775.
  • Tanaka, M., Y. Machida, S. Niu, T. Ikeda, N. R. Jana, H. Doi, M. Kurosawa, M. Nekooki, and N. Nukina. 2004. “Trehalose Alleviates Polyglutamine-Mediated Pathology in a Mouse Model of Huntington Disease.” Nature Medicine 10 (2): 148.
  • 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.
  • Wong, W. 2016. “Limiting Inflammation with P62.” Science Signaling 9 (418): ec52.
  • Wu, Y.-N., L.-X. Yang, X.-Y. Shi, I.-C. Li, J. M. Biazik, K. R. Ratinac, D.-H. Chen., et al. 2011. “The Selective Growth Inhibition of Oral Cancer by Iron Core-Gold Shell Nanoparticles through Mitochondria-Mediated Autophagy.” Biomaterials 32 (20): 4565–4573.
  • Zhang, Q., W. Yang, N. Man, F. Zheng, Y. Shen, K. Sun, Y. Li., et al. 2009. “Autophagy-Mediated Chemosensitization in Cancer Cells by Fullerene C60 Nanocrystal.” Autophagy 5 (8): 1107–1117.

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