Reactive oxygen species damage drives cardiac and mitochondrial dysfunction following acute nano-titanium dioxide inhalation exposure

References

• Arai, M., H. Imai, T. Koumura, M. Yoshida, K. Emoto, M. Umeda, N. Chiba, and Y. Nakagawa. 1999. “Mitochondrial Phospholipid Hydroperoxide Glutathione Peroxidase Plays a Major Role in Preventing Oxidative Injury to Cells.” Journal of Biological Chemistry 274 (8): 4924–4933.
   PubMed Web of Science ®Google Scholar
• Baseler, W. A., E. R. Dabkowski, R. Jagannathan, D. Thapa, C. E. Nichols, D. L. Shepherd, T. L. Croston, et al. 2013. “Reversal of Mitochondrial Proteomic Loss in Type 1 Diabetic Heart with Overexpression of Phospholipid Hydroperoxide Glutathione Peroxidase.” American Journal of Physiology Regulatory Integrative and Comparative Physiology 304 (7): R553–R565.
   PubMed Web of Science ®Google Scholar
• Baseler, W. A., E. R. Dabkowski, C. L. Williamson, T. L. Croston, D. Thapa, M. J. Powell, T. T. Razunguzwa, and J. M. Hollander. 2011. “Proteomic Alterations of Distinct Mitochondrial Subpopulations in the Type 1 Diabetic Heart: contribution of Protein Import Dysfunction.” American Journal of Physiology Regulatory Integrative and Comparative Physiology 300: R186–R200.
   PubMed Web of Science ®Google Scholar
• Bauer, M., S. Cheng, M. Jain, S. Ngoy, C. Theodoropoulos, A. Trujillo, F. C. Lin, and R. Liao. 2011. “Echocardiographic Speckle-Tracking Based Strain Imaging for Rapid Cardiovascular Phenotyping in Mice.” Circulation Research 108 (8): 908–916.
   PubMed Web of Science ®Google Scholar
• Bradford, M. M. 1976. “A Rapid and Sensitive Method for the Quantitation of Microgram Quantities of Protein Utilizing the Principle of Protein-Dye Binding.” Analytical Biochemistry 72 (1–2): 248–254.
   PubMed Web of Science ®Google Scholar
• Chance, B., and G. R. Williams. 1955. “Respiratory Enzymes in Oxidative Phosphorylation. I. Kinetics of Oxygen Utilization.” The Journal of Biological Chemistry 217 (1): 383–393.
   PubMed Web of Science ®Google Scholar
• Chance, B., and G. R. Williams. 1956. “Respiratory Enzymes in Oxidative Phosphorylation. VI. The Effects of Adenosine Diphosphate on Azide-Treated Mitochondria.” The Journal of Biological Chemistry 221: 477–489.
   PubMed Web of Science ®Google Scholar
• Chen, S., J. Yuan, S. Qiao, F. Duan, J. Zhang, and H. Wang. 2014. “Evaluation of Left Ventricular Diastolic Function by Global Strain Rate Imaging in Patients with Obstructive Hypertrophic Cardiomyopathy: A Simultaneous Speckle Tracking Echocardiography and Cardiac Catheterization Study.” Echocardiography 31 (5): 615–622.
   PubMed Web of Science ®Google Scholar
• Chen, Z., Y. Wang, L. Zhuo, S. Chen, L. Zhao, X. Luan, H. Wang, and G. Jia. 2015. “Effect of Titanium Dioxide Nanoparticles on the Cardiovascular System after Oral Administration.” Toxicology Letters 239 (2): 123–130.
   PubMed Web of Science ®Google Scholar
• Cherry, A. D., and C. A. Piantadosi. 2015. “Regulation of Mitochondrial Biogenesis and Its Intersection with Inflammatory Responses.” Antioxidants and Redox Signaling 22 (12): 965–976.
   PubMed Web of Science ®Google Scholar
• Croston, T. L., D. L. Shepherd, D. Thapa, C. E. Nichols, S. E. Lewis, E. R. Dabkowski, R. Jagannathan, W. A. Baseler, and J. M. Hollander. 2013. “Evaluation of the Cardiolipin Biosynthetic Pathway and Its Interactions in the Diabetic Heart.” Life Sciences 93 (8): 313–322.
   PubMed Web of Science ®Google Scholar
• Croston, T. L., D. Thapa, A. A. Holden, K. J. Tveter, S. E. Lewis, D. L. Shepherd, C. E. Nichols, et al. 2014. “Functional Deficiencies of Subsarcolemmal Mitochondria in the Type 2 Diabetic Human Heart.” American Journal of Physiology Heart and Circulatory Physiology 307 (1): H54–H65.
   PubMed Web of Science ®Google Scholar
• Dabkowski, E. R., W. A. Baseler, C. L. Williamson, M. Powell, T. T. Razunguzwa, J. C. Frisbee, and J. M. Hollander. 2010. “Mitochondrial Dysfunction in the Type 2 Diabetic Heart Is Associated with Alterations in Spatially Distinct Mitochondrial Proteomes.” American Journal of Physiology Heart and Circulatory Physiology 299 (2): H529–H540.
   PubMed Web of Science ®Google Scholar
• Dabkowski, E. R., C. L. Williamson, and J. M. Hollander. 2008. “Mitochondria-Specific Transgenic Overexpression of Phospholipid Hydroperoxide Glutathione Peroxidase (GPx4) Attenuates Ischemia/Reperfusion-Associated Cardiac Dysfunction.” Free Radical Biology and Medicine 45 (6): 855–865.
   PubMed Web of Science ®Google Scholar
• Donaldson, K., D. Brown, A. Clouter, R. Duffin, W. Macnee, L. Renwick, L. Tran, and V. Stone. 2002. “The Pulmonary Toxicology of Ultrafine Particles.” Journal of Aerosol Medicine : The Official Journal of the International Society for Aerosols in Medicine 15 (2): 213–220.
   PubMedGoogle Scholar
• Duan, J., Y. Yu, Y. Li, Y. Li, H. Liu, L. Jing, M. Yang, J. Wang, C. Li, and Z. Sun. 2016. “Low-Dose Exposure of Silica Nanoparticles Induces Cardiac Dysfunction via Neutrophil-Mediated Inflammation and Cardiac Contraction in Zebrafish Embryos.” Nanotoxicology 10 (5): 575–585.
   PubMed Web of Science ®Google Scholar
• Elder, A., and G. Oberdorster. 2006. “Translocation and Effects of Ultrafine Particles outside of the Lung.” Clinics in Occupational and Environmental Medicine 5 (4): 785–796.
   PubMedGoogle Scholar
• Elder, A. C., R. Gelein, M. Azadniv, M. Frampton, J. Finkelstein, and G. Oberdorster. 2004. “Systemic Effects of Inhaled Ultrafine Particles in Two Compromised, Aged Rat Strains.” Inhalation Toxicology 16 (6–7): 461–471.
   PubMed Web of Science ®Google Scholar
• Ferin, J., G. Oberdorster, and D. P. Penney. 1992. “Pulmonary Retention of Ultrafine and Fine Particles in Rats.” American Journal of Respiratory Cell and Molecular Biology 6 (5): 535–542.
   PubMed Web of Science ®Google Scholar
• Flarsheim, C. E., I. L. Grupp, and M. A. Matlib. 1996. “Mitochondrial Dysfunction Accompanies Diastolic Dysfunction in Diabetic Rat Heart.” American Journal of Physiology 271: H192–H202.
   PubMed Web of Science ®Google Scholar
• Fu, P. P., Q. Xia, H. M. Hwang, P. C. Ray, and H. Yu. 2014. “Mechanisms of Nanotoxicity: generation of Reactive Oxygen Species.” Journal of Food and Drug Analysis 22 (1): 64–75.
   PubMed Web of Science ®Google Scholar
• Hathaway, Q. A., C. E. Nichols, D. L. Shepherd, P. A. Stapleton, S. L. Mclaughlin, J. C. Stricker, S. L. Rellick, et al. 2016. “Maternal Engineered Nanomaterial Exposure Disrupts Progeny Cardiac Function and Bioenergetics.” American Journal of Physiology Heart and Circulatory Physiology 312 (3): H446–H458.
   PubMed Web of Science ®Google Scholar
• Huerta-Garcia, E., J. A. Perez-Arizti, S. G. Marquez-Ramirez, N. L. Delgado-Buenrostro, Y. I. Chirino, G. G. Iglesias, and R. Lopez-Marure. 2014. “Titanium Dioxide Nanoparticles Induce Strong Oxidative Stress and Mitochondrial Damage in Glial Cells.” Free Radical Biology and Medicine 73: 84–94.
   PubMed Web of Science ®Google Scholar
• Husain, M., A. T. Saber, C. Guo, N. R. Jacobsen, K. A. Jensen, C. L. Yauk, A. Williams, U. Vogel, H. Wallin, and S. Halappanavar. 2013. “Pulmonary Instillation of Low Doses of Titanium Dioxide Nanoparticles in Mice Leads to Particle Retention and Gene Expression Changes in the Absence of Inflammation.” Toxicology and Applied Pharmacology 269 (3): 250–262.
   PubMed Web of Science ®Google Scholar
• Husain, M., D. Wu, A. T. Saber, N. Decan, N. R. Jacobsen, A. Williams, C. L. Yauk, H. Wallin, U. Vogel, and S. Halappanavar. 2015. “Intratracheally Instilled Titanium Dioxide Nanoparticles Translocate to Heart and Liver and Activate Complement Cascade in the Heart of C57BL/6 Mice.” Nanotoxicology 9 (8): 1013–1022.
   PubMed Web of Science ®Google Scholar
• Imai, H., and Y. Nakagawa. 2003. “Biological Significance of Phospholipid Hydroperoxide Glutathione Peroxidase (PHGPx, GPx4) in Mammalian Cells.” Free Radical Biology and Medicine 34 (2): 145–169.
   PubMed Web of Science ®Google Scholar
• Jagannathan, R., D. Thapa, C. E. Nichols, D. L. Shepherd, J. C. Stricker, T. L. Croston, W. A. Baseler, S. E. Lewis, I. Martinez, and J. M. Hollander. 2015. “Translational Regulation of the Mitochondrial Genome following Redistribution of Mitochondrial MicroRNA in the Diabetic Heart.” Circulation: Cardiovascular Genetics 8: 785–802.
   PubMed Web of Science ®Google Scholar
• Ji, L. L., C. Leeuwenburgh, S. Leichtweis, M. Gore, R. Fiebig, J. Hollander, and J. Bejma. 1998. “Oxidative Stress and Aging. Role of Exercise and Its Influences on Antioxidant Systems.” Annals of the New York Academy of Sciences 854: 102–117.
   PubMed Web of Science ®Google Scholar
• Kan, H., Z. Wu, Y. C. Lin, T. H. Chen, J. L. Cumpston, M. L. Kashon, S. Leonard, A. E. Munson, and V. Castranova. 2014. “The Role of Nodose Ganglia in the Regulation of Cardiovascular Function following Pulmonary Exposure to Ultrafine Titanium Dioxide.” Nanotoxicology 8 (4): 447–454.
   PubMed Web of Science ®Google Scholar
• Kan, H., Z. Wu, S. H. Young, T. H. Chen, J. L. Cumpston, F. Chen, M. L. Kashon, and V. Castranova. 2012. “Pulmonary Exposure of Rats to Ultrafine Titanium Dioxide Enhances Cardiac Protein Phosphorylation and Substance P Synthesis in Nodose Ganglia.” Nanotoxicology 6 (7): 736–745.
   PubMed Web of Science ®Google Scholar
• Langrish, J. P., J. Bosson, J. Unosson, A. Muala, D. E. Newby, N. L. Mills, A. Blomberg, and T. Sandstrom. 2012. “Cardiovascular Effects of Particulate Air Pollution Exposure: time Course and Underlying Mechanisms.” Journal of Internal Medicine 272: 224–239.
   PubMed Web of Science ®Google Scholar
• Leblanc, A. J., J. L. Cumpston, B. T. Chen, D. Frazer, V. Castranova, and T. R. Nurkiewicz. 2009. “Nanoparticle Inhalation Impairs Endothelium-Dependent Vasodilation in Subepicardial Arterioles.” Journal of Toxicology Environmental Health Part A 72 (24): 1576–1584.
   PubMed Web of Science ®Google Scholar
• Leblanc, A. J., A. M. Moseley, B. T. Chen, D. Frazer, V. Castranova, and T. R. Nurkiewicz. 2010. “Nanoparticle Inhalation Impairs Coronary Microvascular Reactivity via a Local Reactive Oxygen Species-Dependent Mechanism.” Cardiovascular Toxicology 10 (1): 27–36.
   PubMed Web of Science ®Google Scholar
• Liang, H. Y., S. Cauduro, P. Pellikka, J. Wang, S. Urheim, E. H. Yang, C. Rihal, et al. 2006. “Usefulness of Two-Dimensional Speckle Strain for Evaluation of Left Ventricular Diastolic Deformation in Patients with Coronary Artery Disease.” American Journal of Cardiology 98 (12): 1581–1586.
   PubMed Web of Science ®Google Scholar
• Miller, M. R., C. A. Shaw, and J. P. Langrish. 2012. “From Particles to Patients: oxidative Stress and the Cardiovascular Effects of Air Pollution.” Future Cardiology 8 (4): 577–602.
   PubMedGoogle Scholar
• Mishra, R. K., R. B. Devereux, B. E. Cohen, M. A. Whooley, and N. B. Schiller. 2011. “Prediction of Heart Failure and Adverse Cardiovascular Events in Outpatients with Coronary Artery Disease Using Mitral E/a Ratio in Conjunction with e-Wave Deceleration Time: The Heart and Soul Study.” Journal of the American Society of Echocardiography 24 (10): 1134–1140.
   PubMed Web of Science ®Google Scholar
• Moschini, E., M. Gualtieri, M. Colombo, U. Fascio, M. Camatini, and P. Mantecca. 2013. “The Modality of Cell-Particle Interactions Drives the Toxicity of Nanosized CuO and TiO(2) in Human Alveolar Epithelial Cells.” Toxicology Letter 222 (2): 102–116.
   PubMed Web of Science ®Google Scholar
• Nichols, C. E., D. L. Shepherd, T. L. Knuckles, D. Thapa, J. C. Stricker, P. A. Stapleton, V. C. Minarchick, et al. 2015. “Cardiac and Mitochondrial Dysfunction following Acute Pulmonary Exposure to Mountaintop Removal Mining Particulate Matter.” American Journal of Physiology - Heart and Circulatory Physiology 309 (12): H2017–H2030.
   PubMed Web of Science ®Google Scholar
• Nurkiewicz, T. R., D. W. Porter, A. F. Hubbs, S. Stone, B. T. Chen, D. G. Frazer, M. A. Boegehold, and V. Castranova. 2009. “Pulmonary Nanoparticle Exposure Disrupts Systemic Microvascular Nitric Oxide Signaling.” Toxicological Sciences 110: 191–203.
   Google Scholar
• Oberdorster, G., J. Ferin, and B. E. Lehnert. 1994. “Correlation between Particle Size, in Vivo Particle Persistence, and Lung Injury.” Environmental Health Perspectives, 102 173–179.
   PubMed Web of Science ®Google Scholar
• Oberdorster, G., J. N. Finkelstein, C. Johnston, R. Gelein, C. Cox, R. Baggs, and A. C. Elder. 2000. “Acute Pulmonary Effects of Ultrafine Particles in Rats and Mice.” Research Reports Health Effects Institute 96: 5–74.
   PubMedGoogle Scholar
• Palmer, J. W., B. Tandler, and C. L. Hoppel. 1977. “Biochemical Properties of Subsarcolemmal and Interfibrillar Mitochondria Isolated from Rat Cardiac Muscle.” The Journal of Biological Chemistry 252: 8731–8739.
   PubMed Web of Science ®Google Scholar
• Porter, D. W., A. F. Hubbs, B. T. Chen, W. Mckinney, R. R. Mercer, M. G. Wolfarth, L. Battelli, et al. 2013. “Acute Pulmonary Dose-Responses to Inhaled Multi-Walled Carbon Nanotubes.” Nanotoxicology 7: 1179–1194.
   PubMed Web of Science ®Google Scholar
• Robichaud, C. O., A. E. Uyar, M. R. Darby, L. G. Zucker, and M. R. Wiesner. 2009. “Estimates of Upper Bounds and Trends in Nano-TiO2 Production as a Basis for Exposure Assessment.” Environmental Science and Technology 43 (12): 4227–4233.
   PubMed Web of Science ®Google Scholar
• Roduner, E. 2006. “Size Matters: why Nanomaterials Are Different.” Chemical Society Reviews 35 (7): 583–592.
   PubMed Web of Science ®Google Scholar
• Sarkar, A., M. Ghosh, and P. C. Sil. 2014. “Nanotoxicity: oxidative Stress Mediated Toxicity of Metal and Metal Oxide Nanoparticles.” Journal of Nanoscience and Nanotechnology 14 (1): 730–743.
   PubMed Web of Science ®Google Scholar
• Savi, M., S. Rossi, L. Bocchi, L. Gennaccaro, F. Cacciani, A. Perotti, D. Amidani, et al. 2014. “Titanium Dioxide Nanoparticles Promote Arrhythmias via a Direct Interaction with Rat Cardiac Tissue.” Particle and Fibre Toxicology 11 (1): 63.
   PubMedGoogle Scholar
• Schnurr, K., J. Belkner, F. Ursini, T. Schewe, and H. Kuhn. 1996. “The Selenoenzyme Phospholipid Hydroperoxide Glutathione Peroxidase Controls the Activity of the 15-Lipoxygenase with Complex Substrates and Preserves the Specificity of the Oxygenation Products.” Journal of Biological Chemistry 271: 4653–4658.
   PubMed Web of Science ®Google Scholar
• Sha, B., W. Gao, S. Wang, W. Li, X. Liang, F. Xu, and T. J. Lu. 2013. “Nano-Titanium Dioxide Induced Cardiac Injury in Rat under Oxidative Stress.” Food and Chemical Toxicology 58: 280–288.
   PubMed Web of Science ®Google Scholar
• Sheng, L., X. Wang, X. Sang, Y. Ze, X. Zhao, D. Liu, S. Gui, et al. 2013. “Cardiac Oxidative Damage in Mice following Exposure to Nanoparticulate Titanium Dioxide.” Journal of Biomedical Materials Research Part A 101: 3238–3246.
   PubMed Web of Science ®Google Scholar
• Shepherd, D. L., C. E. Nichols, T. L. Croston, S. L. Mclaughlin, A. B. Petrone, S. E. Lewis, D. Thapa, D. M. Long, G. M. Dick, and J. M. Hollander. 2015. “Early Detection of Cardiac Dysfunction in the Type 1 Diabetic Heart Using Speckle-Tracking Based Strain Imaging.” Journal of Molecular and Cellular Cardiology 90: 74–83.
   PubMed Web of Science ®Google Scholar
• Stapleton, P. A., C. E. Nichols, J. Yi, C. R. Mcbride, V. C. Minarchick, D. L. Shepherd, J. M. Hollander, and T. R. Nurkiewicz. 2015. “Microvascular and Mitochondrial Dysfunction in the Female F1 Generation after Gestational TiO2 Nanoparticle Exposure.” Nanotoxicology 9 (8): 941–951.
   PubMed Web of Science ®Google Scholar
• Thapa, D., C. E. Nichols, S. E. Lewis, D. L. Shepherd, R. Jagannathan, T. L. Croston, K. J. Tveter, A. A. Holden, W. A. Baseler, and J. M. Hollander. 2015. “Transgenic Overexpression of Mitofilin Attenuates Diabetes Mellitus-Associated Cardiac and Mitochondria Dysfunction.” Journal of Molecular and Cellular Cardiology 79: 212–223.
   PubMed Web of Science ®Google Scholar
• Thomas, J. P., M. Maiorino, F. Ursini, and A. W. Girotti. 1990. “Protective Action of Phospholipid Hydroperoxide Glutathione Peroxidase against Membrane-Damaging Lipid Peroxidation. In Situ Reduction of Phospholipid and Cholesterol Hydroperoxides.” The Journal of Biological Chemistry 265: 454–461.
   PubMed Web of Science ®Google Scholar
• Thurn, K. T., T. Paunesku, A. Wu, E. M. Brown, B. Lai, S. Vogt, J. Maser, et al. 2009. “Labeling TiO2 Nanoparticles with Dyes for Optical Fluorescence Microscopy and Determination of TiO2-DNA Nanoconjugate Stability.” Small 5 (11): 1318–1325.
   PubMed Web of Science ®Google Scholar
• Ursini, F., M. Maiorino, and C. Gregolin. 1985. “The Selenoenzyme Phospholipid Hydroperoxide Glutathione Peroxidase.” Biochimica et Biophysica Acta 839 (1): 62–70.
   PubMedGoogle Scholar
• Xia, T., P. Korge, J. N. Weiss, N. Li, M. I. Venkatesen, C. Sioutas, and A. Nel. 2004. “Quinones and Aromatic Chemical Compounds in Particulate Matter Induce Mitochondrial Dysfunction: implications for Ultrafine Particle Toxicity.” Environmental Health Perspectives 112 (14): 1347–1358.
   PubMed Web of Science ®Google Scholar
• Yi, J., B. T. Chen, D. Schwegler-Berry, D. Frazer, V. Castranova, C. Mcbride, T. L. Knuckles, P. A. Stapleton, V. C. Minarchick, and T. R. Nurkiewicz. 2013. “Whole-Body Nanoparticle Aerosol Inhalation Exposures.” Journal of Visucalized Experiments 75:e50263.
   PubMed Web of Science ®Google Scholar
• Zell, R., P. Geck, K. Werdan, and P. Boekstegers. 1997. “TNF-Alpha and IL-1 Alpha Inhibit Both Pyruvate Dehydrogenase Activity and Mitochondrial Function in Cardiomyocytes: evidence for Primary Impairment of Mitochondrial Function.” Molecular and Cellular Biochemistry 177: 61–67.
   PubMed Web of Science ®Google Scholar