Titanium dioxide nanoparticle exposure alters metabolic homeostasis in a cell culture model of the intestinal epithelium and Drosophila melanogaster

References

• Alves, M. B. R., E. C. C. Celeghini, A. F. C. Andrade, R. P. Arruda, L. Batissaco, and T. G. Almeida. 2015. Cellrox deep red® for the detection of oxidative stress in ram sperm by in vitro induction. Animal Reproduction; Animal Reproduction, v 11, n 3 (2014).
   Google Scholar
• Alzaid, F., H. M. Cheung, V. R. Preedy, and P. A. Sharp. 2013. “Regulation of Glucose Transporter Expression in Human Intestinal Caco-2 Cells following Exposure to an Anthocyanin-Rich Berry Extract.” PLoS One 8 (11): e78932.
   PubMed Web of Science ®Google Scholar
• Apidianakis, Y., and L. G. Rahme. 2011. “Drosophila melanogaster as a Model for Human Intestinal Infection and Pathology.” Disease Models & Mechanisms 4 (1): 21–30.
   PubMed Web of Science ®Google Scholar
• Baker, K. D., and C. S. Thummel. 2007. “Diabetic Larvae and Obese Flies – Emerging Studies of Metabolism in Drosophila.” Cell Metabolism 6 (4): 257–266.
   PubMed Web of Science ®Google Scholar
• Barnes, R. J., R. Molina, J. Xu, P. J. Dobson, and I. P. Thompson. 2013. “Comparison of TiO2 and ZnO Nanoparticles for Photocatalytic Degradation of Methylene Blue and the Correlated Inactivation of Gram-Positive and Gram-Negative bacteria.” Journal of Nanoparticle Research 15 (2): 1432.
   Web of Science ®Google Scholar
• Becker, C., A. Hammerle-Fickinger, I. Riedmaier, and M. W. Pfaffl. 2010. “mRNA and microRNA Quality Control for RT-qPCR Analysis.” Methods (San Diego, CA) 50 (4): 237–243.
   PubMed Web of Science ®Google Scholar
• Bergin, I. L., L. A. Wilding, M. Morishita, K. Walacavage, A. P. Ault, J. L. Axson, D.I. Stark, et al. 2016. “Effects of particle size and coating on toxicologic parameters, fecal elimination kinetics and tissue distribution of acutely ingested silver nanoparticles in a mouse model.” Nanotoxicology 10(3):352–360.
   PubMed Web of Science ®Google Scholar
• Blodgett, A. B., R. K. Kothinti, I. Kamyshko, D. H. Petering, S. Kumar, and N. M. Tabatabai. 2011. “A Fluorescence Method for Measurement of Glucose Transport in Kidney Cells.” Diabetes Technology & Therapeutics 13 (7): 743–751.
   PubMed Web of Science ®Google Scholar
• Borgström, B.,. A. Dahlqvist, G. Lundh, and J. Sjövall. 1957. “Studies of Intestinal Digestion and Absorption in the Human.” Journal of Clinical Investigation 36 (10): 1521–1536.
   PubMed Web of Science ®Google Scholar
• Brown, R. P., M. D. Delp, S. L. Lindstedt, L. R. Rhomberg, and R. P. Beliles. 1997. “Physiological Parameter Values for Physiologically Based Pharmacokinetic Models.” Toxicology and Industrial Health 13 (4): 407–484.
   PubMed Web of Science ®Google Scholar
• Brun, E., F. Barreau, G. Veronesi, B. Fayard, S. Sorieul, C. Chaneac, C. Carapito, et al. 2014. “Titanium Dioxide Nanoparticle Impact and Translocation through Ex Vivo, in Vivo and in Vitro Gut Epithelia.” Particle and Fibre Toxicology  11: 13.
   Google Scholar
• Chen, H., R. Zhao, B. Wang, C. Cai, L. Zheng, H. Wang, M. Wang, et al. 2017. “The Effects of Orally Administered Ag, TiO2 and SiO2 Nanoparticles on Gut Microbiota Composition and Colitis Induction in Mice.” NanoImpact 8: 80–88.
   Web of Science ®Google Scholar
• Cho, W. S., B. C. Kang, J. K. Lee, J. Jeong, J. H. Che, and S. H. Seok. 2013. “Comparative Absorption, Distribution, and Excretion of Titanium Dioxide and Zinc Oxide Nanoparticles after Repeated Oral Administration.” Particle and Fibre Toxicology 10: 9.
   Google Scholar
• Chow, J., S. M. Lee, Y. Shen, A. Khosravi, and S. K. Mazmanian. 2010. “Host–Bacterial Symbiosis in Health and Disease.” Advances in Immunology 107: 243–274.
   PubMed Web of Science ®Google Scholar
• Cline, G. W., K. F. Petersen, M. Krssak, J. Shen, R. S. Hundal, Z. Trajanoski, S. Inzucchi, A. Dresner, D. L. Rothman, and G. I. Shulman. 1999. “Impaired Glucose Transport as a Cause of Decreased Insulin-Stimulated Muscle Glycogen Synthesis in Type 2 Diabetes.” New England Journal of Medicine 341 (4): 240–246.
   PubMed Web of Science ®Google Scholar
• DeSesso, J. M., and C. F. Jacobson. 2001. “Anatomical and Physiological Parameters Affecting Gastrointestinal Absorption in Humans and Rats.” Food and Chemical Toxicology 39 (3): 209–228.
   PubMed Web of Science ®Google Scholar
• Dizaj, S. M., F. Lotfipour, M. Barzegar-Jalali, M. H. Zarrintan, and K. Adibkia. 2014. “Antimicrobial Activity of the Metals and Metal Oxide Nanoparticles.” Materials Science & Engineering C, Materials for Biological Applications 44: 278–284.
   PubMed Web of Science ®Google Scholar
• Fondevila, M., R. Herrer, M. C. Casallas, L. Abecia, and J. J. Ducha. 2009. “Silver Nanoparticles as a Potential Antimicrobial Additive for Weaned Pigs.” Animal Feed Science and Technology 150 (3–4): 259–269.
   Web of Science ®Google Scholar
• Francavilla, R., V. Miniello, A. M. Magista, A. De Canio, N. Bucci, F. Gagliardi, E. Lionetti, et al. 2010. “A Randomized Controlled Trial of Lactobacillus GG in Children with Functional Abdominal Pain.” Pediatrics 126 (6): e1445–e1452.
   PubMed Web of Science ®Google Scholar
• Fu, G., P. S. Vary, and C. T. Lin. 2005. “Anatase TiO2 Nanocomposites for Antimicrobial Coatings.” The Journal of Physical Chemistry B 109 (18): 8889–8898.
   PubMed Web of Science ®Google Scholar
• Guarner, F., and J.-R. Malagelada. 2003. “Gut Flora in Health and Disease.” Lancet (London, England) 361 (9356): 512–519.
   PubMed Web of Science ®Google Scholar
• Guo, Z., N. J. Martucci, F. Moreno-Olivas, E. Tako, and G. J. Mahler. 2017. “Titanium Dioxide Nanoparticle Ingestion Alters Nutrient Absorption in an in Vitro Model of the Small Intestine.” NanoImpact 5: 70–82.
   PubMed Web of Science ®Google Scholar
• Hadrup, N., K. Loeschner, A. Bergström, A. Wilcks, X. Gao, U. Vogel, H. L. Frandsen, E. H. Larsen, H. R. Lam, and A. Mortensen. 2012. “Subacute Oral Toxicity Investigation of Nanoparticulate and Ionic Silver in Rats.” Archives of Toxicology 86 (4): 543.
   PubMed Web of Science ®Google Scholar
• Hothorn, T., F. Bretz, and P. Westfall. 2008. “Simultaneous Inference in General Parametric Models.” Biometrical Journal 50 (3): 346–363.
   PubMed Web of Science ®Google Scholar
• Jiang, W., K. Yang, R. W. Vachet, and B. Xing. 2010. “Interaction between Oxide Nanoparticles and Biomolecules of the Bacterial Cell Envelope as Examined by Infrared Spectroscopy.” Langmuir: The ACS Journal of Surfaces and Colloids 26 (23): 18071–18077.
   PubMed Web of Science ®Google Scholar
• Johnson-Henry, K. C., K. A. Donato, G. Shen-Tu, M. Gordanpour, and P. M. Sherman. 2008. “Lactobacillus rhamnosus Strain GG Prevents Enterohemorrhagic Escherichia coli O157:H7-Induced Changes in Epithelial Barrier Function.” Infection and Immunity 76 (4): 1340–1348.
   PubMed Web of Science ®Google Scholar
• Jovanović, B., V. J. Cvetković, and T. L. Mitrović. 2016. “Effects of Human Food Grade Titanium Dioxide Nanoparticle Dietary Exposure on Drosophila melanogaster Survival, Fecundity, Pupation and Expression of Antioxidant Genes.” Chemosphere 144: 43–49.
   PubMed Web of Science ®Google Scholar
• Kipp, H., S. Khoursandi, D. Scharlau, and R. K. Kinne. 2003. “More than Apical: Distribution of SGLT1 in Caco-2 Cells.” American Journal of Physiology Cell Physiology 285 (4): C737–C749.
   PubMed Web of Science ®Google Scholar
• Koeneman, B. A., Y. Zhang, P. Westerhoff, Y. Chen, J. C. Crittenden, and D. G. Capco. 2010. “Toxicity and Cellular Responses of Intestinal Cells Exposed to Titanium Dioxide.” Cell Biology and Toxicology 26 (3): 225–238.
   PubMed Web of Science ®Google Scholar
• Krüger, K., K. Schrader, and M. Klempt. 2017. “Cellular Response to Titanium Dioxide Nanoparticles in Intestinal Epithelial Caco-2 Cells Is Dependent on Endocytosis-Associated Structures and Mediated by EGFR.” Nanomaterials 7 (4): 79.
   Web of Science ®Google Scholar
• Kubacka, A., M. S. Diez, D. Rojo, R. Bargiela, S. Ciordia, I. Zapico, J. P. Albar, et al. 2015. “Understanding the Antimicrobial Mechanism of TiO(2)-Based Nanocomposite Films in a Pathogenic Bacterium.” Scientific Reports 4 (1): 4134.
   Google Scholar
• Lee, H. H., A. S. Prasad, G. J. Brewer, and C. Owyang. 1989. “Zinc Absorption in Human Small Intestine.” American Journal of Physiology – Gastrointestinal and Liver Physiology 256 (1): G87–G91.
   Google Scholar
• Leopold, P., and N. Perrimon. 2007. “Drosophila and the Genetics of the Internal Milieu.” Nature 450 (7167): 186–188.
   PubMed Web of Science ®Google Scholar
• Lesuffleur, T., A. Barbat, E. Dussaulx, and A. Zweibaum. 1990. “Growth Adaptation to Methotrexate of HT-29 Human Colon-Carcinoma Cells Is Associated with Their Ability to Differentiate into Columnar Absorptive and Mucus-Secreting Cells.” Cancer Research 50: 6334–6343.
   PubMed Web of Science ®Google Scholar
• Lewandowski, A. T., W. E. Bentley, H. Yi, G. W. Rubloff, G. F. Payne, and R. Ghodssi. 2008. “Towards Area-Based in Vitro Metabolic Engineering: Assembly of Pfs Enzyme onto Patterned Microfabricated Chips.” Biotechnology Progress 24 (5): 1042–1051.
   PubMed Web of Science ®Google Scholar
• Ley, R. E., M. Hamady, C. Lozupone, P. J. Turnbaugh, R. R. Ramey, J. S. Bircher, M. L. Schlegel, et al. 2008. “Evolution of Mammals and Their Gut Microbes.” Science (New York, N.Y.) 320 (5883): 1647–1651.
   PubMed Web of Science ®Google Scholar
• Livak, K. J., and T. D. Schmittgen. 2001. “Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2(-Delta Delta C(T)) Method.” Methods (San Diego, Calif) 25 (4): 402–408.
   PubMed Web of Science ®Google Scholar
• Lo Giudice, M. C., L. M. Herda, E. Polo, and K. A. Dawson. 2016. “In Situ Characterization of Nanoparticle Biomolecular Interactions in Complex Biological Media by Flow Cytometry.” Nature Communications 7: 13475.
   PubMed Web of Science ®Google Scholar
• Lomer, M. C. E., R. P. H. Thompson, and J. J. Powell. 2002. “Fine and Ultrafine Particles of the Diet: Influence on the Mucosal Immune Response and Association with Crohn’s Disease.” Proceedings of the Nutrition Society 61 (01): 123–130.
   PubMedGoogle Scholar
• Ludwig, D. S. 2002. “The Glycemic Index: Physiological Mechanisms Relating to Obesity, Diabetes, and Cardiovascular Disease.” JAMA 287 (18): 2414–2423.
   PubMed Web of Science ®Google Scholar
• Mahida, Y. R., K. C. Wu, and D. P. Jewell. 1989. “Respiratory Burst Activity of Intestinal Macrophages in Normal and Inflammatory Bowel Disease.” Gut 30 (10): 1362–1370.
   PubMed Web of Science ®Google Scholar
• Mahler, G. J., M. L. Shuler, and R. P. Glahn. 2009. “Characterization of Caco-2 and HT29-MTX Cocultures in an in Vitro Digestion/Cell Culture Model Used to Predict Iron Bioavailability.” The Journal of Nutritional Biochemistry 20 (7): 494.
   PubMed Web of Science ®Google Scholar
• Maynard, A. D. 2006. “Nanotechnology: Assessing the Risks.” Nano Today 1 (2): 22–33.
   Web of Science ®Google Scholar
• McGraw, L. A., A. C. Fiumera, M. Ramakrishnan, S. Madhavarapu, A. G. Clark, and M. F. Wolfner. 2007. “Larval Rearing Environment Affects Several Post-Copulatory Traits in Drosophila melanogaster.” Biology Letters 3 (6): 607–610.
   PubMed Web of Science ®Google Scholar
• Mudunkotuwa, I. A., and V. H. Grassian. 2015. “Biological and Environmental Media Control Oxide Nanoparticle Surface Composition: The Roles of Biological Components (Proteins and Amino Acids), Inorganic Oxyanions and Humic Acid.” Environmental Science: Nano 2 (5): 429–439.
   Web of Science ®Google Scholar
• Muir, A., and U. Hopfer. 1985. “Regional Specificity of Iron Uptake by Small Intestinal Brush-Border Membranes from Normal and Iron-Deficient Mice.” American Journal of Physiology: Gastrointestinal and Liver Physiology 248 (3): G376–G379.
   Web of Science ®Google Scholar
• Musselman, L. P., J. L. Fink, K. Narzinski, P. V. Ramachandran, S. S. Hathiramani, R. L. Cagan, and T. J. Baranski. 2011. “A High-Sugar Diet Produces Obesity and Insulin Resistance in Wild-Type Drosophila.” Disease Models & Mechanisms 4: 842–849.
   PubMed Web of Science ®Google Scholar
• Narai, A., S. Arai, and M. Shimizu. 1997. “Rapid Decrease in Transepithelial Electrical Resistance of Human Intestinal Caco-2 Cell Monolayers by Cytotoxic Membrane Perturbents.” Toxicology In Vitro 11 (4): 347.
   PubMed Web of Science ®Google Scholar
• Novak, E. A., and K. P. Mollen. 2015. “Mitochondrial Dysfunction in Inflammatory Bowel Disease.” Frontiers in Cell and Developmental Biology 3: 62.
   PubMed Web of Science ®Google Scholar
• O'Hara, A. M., and F. Shanahan. 2006. “The Gut Flora as a Forgotten Organ.” EMBO Reports 7: 688–693.
   PubMed Web of Science ®Google Scholar
• Philbrook, N. A., L. M. Winn, A. R. M. N. Afrooz, N. B. Saleh, and V. K. Walker. 2011. “The Effect of TiO(2) and Ag Nanoparticles on Reproduction and Development of Drosophila melanogaster and CD-1 Mice.” Toxicology and Applied Pharmacology 257 (3): 429–436.
   PubMed Web of Science ®Google Scholar
• Pielmeier, U., S. Andreassen, B. S. Nielsen, J. G. Chase, and P. Haure. 2010. “A Simulation Model of Insulin Saturation and Glucose Balance for Glycemic Control in ICU Patients.” Computer Methods and Programs in Biomedicine 97 (3): 211–222.
   PubMed Web of Science ®Google Scholar
• Posgai, R., C. B. Cipolla-McCulloch, K. R. Murphy, S. M. Hussain, J. J. Rowe, and M. G. Nielsen. 2011. “Differential Toxicity of Silver and Titanium Dioxide Nanoparticles on Drosophila melanogaster Development, Reproductive Effort, and Viability: Size, Coatings and Antioxidants Matter.” Chemosphere 85 (1): 34–42.
   PubMed Web of Science ®Google Scholar
• Reaven, G. M. 1988. “Banting Lecture 1988. Role of Insulin Resistance in Human Disease.” Diabetes 37 (12): 1595–1607.
   PubMed Web of Science ®Google Scholar
• Ridley, E. V., A. C. Wong, S. Westmiller, and A. E. Douglas. 2012. “Impact of the Resident Microbiota on the Nutritional Phenotype of Drosophila melanogaster.” PLoS One 7 (5): e36765.
   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 & Technology 43 (12): 4227–4233.
   PubMed Web of Science ®Google Scholar
• Schneider, C. A., W. S. Rasband, and K. W. Eliceiri. 2012. “NIH Image to ImageJ: 25 Years of Image Analysis.” Nature Methods 9 (7): 671–675.
   PubMed Web of Science ®Google Scholar
• Sekirov, I., S. L. Russell, L. C. M. Antunes, and B. B. Finlay. 2010. “Gut Microbiota in Health and Disease.” Physiological Reviews 90 (3): 859–904.
   PubMed Web of Science ®Google Scholar
• Seth, A., F. Yan, D. Polk, and R. K. Rao. 2008. “Probiotics Ameliorate the Hydrogen Peroxide-Induced Epithelial Barrier Disruption by a PKC- and MAP Kinase-Dependent Mechanism.” American Journal of Physiology – Gastrointestinal and Liver Physiology 294 (4): G1060–G1069.
   PubMed Web of Science ®Google Scholar
• Shin, S. C., S. H. Kim, H. You, B. Kim, A. C. Kim, K. A. Lee, J. H. Yoon, J. H. Ryu, and W. J. Lee. 2011. “Drosophila Microbiome Modulates Host Developmental and Metabolic Homeostasis via Insulin Signaling.” Science 334 (6056): 670–674.
   PubMed Web of Science ®Google Scholar
• Storelli, G., A. Defaye, B. Erkosar, P. Hols, J. Royet, and F. Leulier. 2011. “Lactobacillus plantarum Promotes Drosophila Systemic Growth by Modulating Hormonal Signals through TOR-Dependent Nutrient Sensing.” Cell Metabolism 14 (3): 403–414.
   PubMed Web of Science ®Google Scholar
• Tallkvist, J., C. L. Bowlus, and B. Lonnerdal. 2000. “Functional and Molecular Responses of Human Intestinal Caco-2 Cells to Iron Treatment.” The American Journal of Clinical Nutrition 72 (3): 770–775.
   PubMed Web of Science ®Google Scholar
• Team, R. C. 2014. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing, 2013.
   Google Scholar
• Tenzer, S., D. Docter, J. Kuharev, A. Musyanovych, V. Fetz, R. Hecht, F. Schlenk, et al. 2013. “Rapid Formation of Plasma Protein Corona Critically Affects Nanoparticle Pathophysiology.” Nature Nanotechnology 8 (10): 772–781.
   PubMed Web of Science ®Google Scholar
• Tong, T., C. T. Binh, J. J. Kelly, J. F. Gaillard, and K. A. Gray. 2013. “Cytotoxicity of Commercial Nano-TiO2 to Escherichia coli Assessed by High-Throughput Screening: Effects of Environmental Factors.” Water Research 47 (7): 2352–2362.
   PubMed Web of Science ®Google Scholar
• US Department of Agriculture and Office of Communications 2003. Chapter 2 Profiling Food Consumption in America. Agriculture Fact Book 2001–2002.
   Google Scholar
• Walter, E., S. Janich, B. J. Roessler, J. M. Hilfinger, and G. L. Amidon. 1996. “HT29-MTX/Caco-2 Cocultures as an in Vitro Model for the Intestinal Epithelium: In Vitro-in Vivo Correlation with Permeability Data from Rats and Humans.” Journal of Pharmaceutical Sciences 85 (10): 1070–1076.
   PubMed Web of Science ®Google Scholar
• Wang, J., G. Zhou, C. Chen, H. Yu, T. Wang, Y. Ma, G. Jia, et al. 2007. “Acute Toxicity and Biodistribution of Different Sized Titanium Dioxide Particles in Mice after Oral Administration.” Toxicology Letters 168 (2): 176–185.
   PubMed Web of Science ®Google Scholar
• Wang, Y., Y. Liu, A. Sidhu, Z. Ma, C. McClain, and W. Feng. 2012. “Lactobacillus rhamnosus GG Culture Supernatant Ameliorates Acute Alcohol-Induced Intestinal Permeability and Liver Injury.” American Journal of Physiology – Gastrointestinal and Liver Physiology 303 (1): G32–G41.
   PubMed Web of Science ®Google Scholar
• Weir, A., P. Westerhoff, L. Fabricius, K. Hristovski, and N. von Goetz. 2012. “Titanium Dioxide Nanoparticles in Food and Personal Care Products.” Environmental Science & Technology 46 (4): 2242–2250.
   PubMed Web of Science ®Google Scholar
• Wikman-Larhed, A., and P. Artursson. 1995. “Cocultures of Human Intestinal Goblet (Ht29-H) and Absorptive (Caco-2) Cells for Studies of Drug and Peptide Absorption.” European Journal of Pharmaceutical Sciences 3 (3): 171–183.
   Web of Science ®Google Scholar
• Xia, T., N. Li, and A. E. Nel. 2009. “Potential Health Impact of Nanoparticles.” Annual Review of Public Health 30 (1): 137–150.
   PubMed Web of Science ®Google Scholar