Tissue biodistribution of intravenously administrated titanium dioxide nanoparticles revealed blood-brain barrier clearance and brain inflammation in rat

Particle and Fibre Toxicology

Volumn 12, Issue 1, 2015, Pages

  Disdier, Clémence ^a   Devoy, Jérôme ^b   Cosnefroy, Anne ^a   Chalansonnet, Monique ^b   Herlin Boime, Nathalie ^c   Brun, Emilie ^d   Lund, Amie ^e   Mabondzo, Aloïse ^a  

^a Institut National de la Recherche Agronomique   (France)

^b INSTITUT NATIONAL DE RECHERCHE ET DE SÉCURITÉ   (France)

^c CNRS UMR 3299   (France)

^d UNIVERSITÉ PARIS SUD   (France)

^e UNIVERSITY OF NORTH TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BREAST CANCER RESISTANCE PROTEIN; CLAUDIN 5; CXCL1 CHEMOKINE; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 1BETA; MULTIDRUG RESISTANCE PROTEIN; OCCLUDIN; TITANIUM DIOXIDE NANOPARTICLE; METAL NANOPARTICLE; TITANIUM; TITANIUM DIOXIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOACCUMULATION; BLOOD BRAIN BARRIER; BRAIN CAPILLARY ENDOTHELIAL CELL; CONTROLLED STUDY; ENCEPHALITIS; IMMUNOHISTOCHEMISTRY; LIVER; LUNG; MALE; MASS SPECTROMETRY; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SPLEEN; TISSUE DISTRIBUTION; ANIMAL; CHEMICALLY INDUCED; INTRAVENOUS DRUG ADMINISTRATION;

ANIMALS; BLOOD-BRAIN BARRIER; ENCEPHALITIS; INJECTIONS, INTRAVENOUS; METAL NANOPARTICLES; RATS; TISSUE DISTRIBUTION; TITANIUM;

EID: 84940660873     PISSN: 17438977     EISSN: 17438977     Source Type: Journal    
DOI: 10.1186/s12989-015-0102-8     Document Type: Article

References (58)

1. Chen X, Mao SS. Titanium dioxide nanomaterials: synthesis, properties, modifications, and applications. Chem Rev. 2007;107:2891-959.
2. Weir A, Westerhoff P, Fabricius L, Hristovski K, von Goetz N. Titanium dioxide nanoparticles in food and personal care products. Environ Sci Technol. 2012;46:2242-50.
3. Peters RJB, van Bemmel G, Herrera-Rivera Z, Helsper HPFG, Marvin HJP, Weigel S, et al. Characterization of titanium dioxide nanoparticles in food products: analytical methods to define nanoparticles. J Agric Food Chem. 2014;62:6285-93.
4. Brun E, Barreau F, Veronesi G, Fayard B, Sorieul S, Chaneac C, et al. Titanium dioxide nanoparticle impact and translocation through ex vivo, in vivo and in vitro gut epithelia. Part Fibre Toxicol. 2014;11:13.
5. Shi H, Magaye R, Castranova V, Zhao J. Titanium dioxide nanoparticles: a review of current toxicological data. Part Fibre Toxicol. 2013;10:15.
6. Iavicoli I, Leso V, Bergamaschi A. Toxicological effects of titanium dioxide nanoparticles: a review of in vivo studies. Journal of Nanomaterials. 2012;15(5):481-508.
7. Abbott NJ, Ronnback L, Hansson E. Astrocyte-endothelial interactions at the blood-brain barrier. Nat Rev Neurosci. 2006;7:41-53.
8. Abbott NJ, Patabendige AAK, Dolman DEM, Yusof SR, Begley DJ. Structure and function of the blood-brain barrier. Neurobiol Dis. 2010;37:13-25.
9. Abbott NJ, Friedman A. Overview and introduction: the blood-brain barrier in health and disease. Epilepsia. 2012;53:1-6.
10. Abbott NJ. Blood-brain barrier structure and function and the challenges for CNS drug delivery. J Inherit Metab Dis. 2013;36:437-49.
11. Keller A. Breaking and building the wall: the biology of the blood-brain barrier in health and disease. Swiss Med Wkly. 2013;143:w13892.
12. Begley DJ. ABC transporters and the blood-brain barrier. Curr Pharm Des. 2004;10:1295-312.
13. Loscher W, Potschka H. Role of drug efflux transporters in the brain for drug disposition and treatment of brain diseases. Prog Neurobiol. 2005;76:22-76.
14. Omidi Y, Barar J. Impacts of blood-brain barrier in drug delivery and targeting of brain tumors. BioImpacts. 2012;2:5-22.
15. Fabian E, Landsiedel R, Ma-Hock L, Wiench K, Wohlleben W, van Ravenzwaay B. Tissue distribution and toxicity of intravenously administered titanium dioxide nanoparticles in rats. Arch Toxicol. 2008;82:151-7.
16. Shinohara N, Danno N, Ichinose T, Sasaki T, Fukui H, Honda K, et al. Tissue distribution and clearance of intravenously administered titanium dioxide (TiO(2)) nanoparticles. Nanotoxicology. 2013;8(2):132-41.
17. Xie G, Wang C, Sun J, Zhong G. Tissue distribution and excretion of intravenously administered titanium dioxide nanoparticles. Toxicol Lett. 2011;205:55-61.
18. Geraets L, Oomen AG, Krystek P, Jacobsen NR, Wallin H, Laurentie M, et al. Tissue distribution and elimination after oral and intravenous administration of different titanium dioxide nanoparticles in rats. Part Fibre Toxicol. 2014;11:30.
19. Wang J, Zhou G, Chen C, Yu H, Wang T, Ma Y, et al. Acute toxicity and biodistribution of different sized titanium dioxide particles in mice after oral administration. Toxicol Lett. 2007;168:176-85.
20. Wang J, Chen C, Liu Y, Jiao F, Li W, Lao F, et al. Potential neurological lesion after nasal instillation of TiO(2) nanoparticles in the anatase and rutile crystal phases. Toxicol Lett. 2008;183:72-80.
21. Takahashi Y, Mizuo K, Shinkai Y, Oshio S, Takeda K. Prenatal exposure to titanium dioxide nanoparticles increases dopamine levels in the prefrontal cotex and neostriatum of mice. J Toxicol Sci. 2010;35:749-56.
22. Shin JA, Lee EJ, Seo SM, Kim HS, Kang JL, Park EM. Nanosized titanium dioxide enhanced inflammatory responses in the septic brain of mouse. Neuroscience. 2010;165:445-54.
23. Ze Y, Zheng L, Zhao X, Gui S, Sang X, Su J, et al. Molecular mechanism of titanium dioxide nanoparticles-induced oxidative injury in the brain of mice. Chemosphere. 2013;92:1183-9.
24. Ze Y, Hu R, Wang X, Sang X, Ze X, Li B, et al. Neurotoxicity and gene-expressed profile in brain-injured mice caused by exposure to titanium dioxide nanoparticles. J Biomed Mater Res A. 2014;102:470-8.
25. Shrivastava R, Raza S, Yadav A, Kushwaha P, Flora SJS. Effects of sub-acute exposure to TiO2, ZnO and Al2O3 nanoparticles on oxidative stress and histological changes in mouse liver and brain. Drug Chem Toxicol. 2014;37:336-47.
26. Lacombe O, Videau O, Chevillon D, Guyot A-C, Contreras C, Blondel S, et al. In vitro primary human and animal cell-based blood-brain barrier models as a screening tool in drug discovery. Mol Pharm. 2011;8:651-63.
27. Brun E, Carriere M, Mabondzo A. In vitro evidence of dysregulation of blood-brain barrier function after acute and repeated/long-term exposure to TiO(2) nanoparticles. Biomaterials. 2012;33:886-96.
28. van Ravenzwaay B, Landsiedel R, Fabian E, Burkhardt S, Strauss V, Ma-Hock L. Comparing fate and effects of three particles of different surface properties: nano-TiO2, pigmentary TiO2 and quartz. Toxicol Lett. 2009;186:152-9.
29. Harati R, Benech H, Villegier AS, Mabondzo A. P-Glycoprotein, breast cancer resistance protein, organic anion transporter 3, and transporting peptide 1a4 during blood-brain barrier maturation: involvement of Wnt/beta-Catenin and Endothelin-1 signaling. Mol Pharm. 2013;10:1566-80.
30. Daneman R. The blood-brain barrier in health and disease. Ann Neurol. 2012;72:648-72.
31. van Vliet EA, Araujo SC, Redeker S, van Schaik R, Aronica E, Gorter JA. Blood-brain barrier leakage may lead to progression of temporal lobe epilepsy. Brain. 2007;130:521-34.
32. Marchi N, Granata T, Alexopoulos A, Janigro D. The blood-brain barrier hypothesis in drug resistant epilepsy. Brain. 2012;135(Pt 4):e211.
33. Hellinger E, Veszelka S, Toth AE, Walter F, Kittel A, Bakk ML, et al. Comparison of brain capillary endothelial cell-based and epithelial (MDCK-MDR1, Caco-2, and VB-Caco-2) cell-based surrogate blood-brain barrier penetration models. Eur J Pharm Biopharm. 2012;82:340-51.
34. Wang X, Campos CR, Peart JC, Smith LK, Boni JL, Cannon RE, et al. Nrf2 upregulates ATP binding cassette transporter expression and activity at the blood-brain and blood-spinal cord barriers. J Neurosci. 2014;34:8585-93.
35. Sugimoto H, Hirabayashi H, Amano N, Moriwaki T. Retrospective analysis of P-Glycoprotein-Mediated Drug-drug interactions at the blood-brain barrier in humans. Drug Metab Dispos. 2013;41:683-8.
36. Schinkel AH, Wagenaar E, Vandeemter L, Mol C, Borst P. Absence of the MDR1A P-Glycoprotein in mice affects tissue distribution and pharmacokinetics of dexamethasone, digoxin, and cyclosporine-A. J Clin Invest. 1995;96:1698-705.
37. Schinkel AH, Mayer U, Wagenaar E, Mol C, van Deemter L, Smit JJM, et al. Normal viability and altered pharmacokinetics in mice lacking mdr1-type (drug-transporting) P-glycoproteins (vol 94, pg 4028, 1997). Proc Natl Acad Sci U S A. 2003;100:8036-6.
38. Mayer U, Wagenaar E, Dorobek B, Beijnen JH, Borst P, Schinkel AH. Full blockade of intestinal P-glycoprotein and extensive inhibition of blood-brain barrier P-glycoprotein by oral treatment of mice with PSC833. J Clin Invest. 1997;100:2430-6.
39. Liu Y-C, Liu H-Y, Yang H-W, Wen T, Shang Y, Liu X-D, et al. Impaired expression and function of breast cancer resistance protein (Bcrp) in brain cortex of streptozocin-induced diabetic rats. Biochem Pharmacol. 2007;74:1766-72.
40. Hartz AMS, Bauer B, Fricker G, Miller DS. Rapid modulation of p-glycoprotein-mediated transport at the blood-brain barrier by tumor necrosis factor-alpha and lipopolysaccharide. Mol Pharmacol. 2006;69:462-70.
41. Miller DS. Regulation of ABC transporters blood-brain barrier: the good, the bad, and the ugly. Adv Cancer Res. 2015;125:43-70.
42. Ma L, Liu J, Li N, Wang J, Duan Y, Yan J, et al. Oxidative stress in the brain of mice caused by translocated nanoparticulate TiO2 delivered to the abdominal cavity. Biomaterials. 2010;31:99-105.
43. Carvalho da Fonseca AC, Matias D, Garcia C, Amaral R, Geraldo LH, Freitas C, et al. The impact of microglial activation on blood-brain barrier in brain diseases. Front Cell Neurosci. 2014;8:362.
44. Miller DS. Regulation of P-glycoprotein and other ABC drug transporters at the blood-brain barrier. Trends Pharmacol Sci. 2010;31:246-54.
45. Bauer B, Hartz AMS, Miller DS. Tumor necrosis factor alpha and endothelin-1 increase P-glycoprotein expression and transport activity at the blood-brain barrier. Mol Pharmacol. 2007;71:667-75.
46. Sha B, Gao W, Wang S, Gou X, Li W, Liang X, et al. Oxidative stress increased hepatotoxicity induced by nano-titanium dioxide in BRL-3A cells and Sprague-Dawley rats. J Appl Toxicol. 2014;34:345-56.
47. Wang Y, Chen ZJ, Ba T, Pu J, Cui XX, Jia G. Effects of TiO2 nanoparticles on antioxidant function and element content of liver and kidney tissues in young and adult rats. Journal of Peking University Health sciences. 2014;46:395-9.
48. Hong J, Wang L, Zhao X, Yu X, Sheng L, Xu B, et al. Th2 factors may be involved in TiO2 NP-induced hepatic inflammation. J Agric Food Chem. 2014;62:6871-8.
49. Didier N, Romero IA, Creminon C, Wijkhuisen A, Grassi J, Mabondzo A. Secretion of interleukin-1 beta by astrocytes mediates endothelin-1 and tumour necrosis factor-alpha effects on human brain microvascular endothelial cell permeability. J Neurochem. 2003;86:246-54.
50. Argaw AT, Zhang Y, Snyder BJ, Zhao M-L, Kopp N, Lee SC, et al. IL-1beta regulates blood-brain barrier permeability via reactivation of the hypoxia-angiogenesis program. J Immunol. 2006;177:5574-84.
51. Labus J, Haeckel S, Lucka L, Danker K. Interleukin-1 beta induces an inflammatory response and the breakdown of the endothelial cell layer in an improved human THBMEC-based in vitro blood-brain barrier model. J Neurosci Methods. 2014;228:35-45.
52. Poller B, Drewe J, Krahenbuhl S, Huwyler J, Gutmann H. Regulation of BCRP (ABCG2) and P-glycoprotein (ABCB1) by cytokines in a model of the human blood-brain barrier. Cell Mol Neurobiol. 2010;30:63-70.
53. Zhang K, Tian L, Liu L, Feng Y, Dong Y-B, Li B, et al. CXCL1 contributes to beta-Amyloid-induced transendothelial migration of monocytes in Alzheimer's disease. PloS One. 2013;8(8):e72744.
54. Campbell IL, Erta M, Lim SL, Frausto R, May U, Rose-John S, et al. Trans-signaling is a dominant mechanism for the pathogenic actions of Interleukin-6 in the brain. J Neurosci. 2014;34:2503-13.
55. Harati R, Villegier A-S, Banks WA, Mabondzo A. Susceptibility of juvenile and adult blood-brain barrier to endothelin-1: regulation of P-glycoprotein and breast cancer resistance protein expression and transport activity. J Neuroinflammation. 2012;9:273.
56. Cecchelli R, Berezowski V, Lundquist S, Culot M, Renftel M, Dehouck M-P, et al. Modelling of the blood-brain barrier in drug discovery and development. Nat Rev Drug Discov. 2007;6:650-61.
57. Deli MA, Abraham CS, Kataoka Y, Niwa M. Permeability studies on in vitro blood-brain barrier models: physiology, pathology, and pharmacology. Cell Mol Neurobiol. 2005;25:59-127.
58. Reichel A, Begley DJ, Abbott NJ. An overview of in vitro techniques for blood-brain barrier studies. Methods Mol Med. 2003;89:307-24.