Titanium dioxide particle type and concentration influence the inflammatory response in Caco-2 cells

International Journal of Molecular Sciences

Volumn 17, Issue 4, 2016, Pages

  Tada Oikawa, Saeko ^a,b   Ichihara, Gaku ^c   Fukatsu, Hitomi ^a   Shimanuki, Yuka ^a   Tanaka, Natsuki ^a   Watanabe, Eri ^c   Suzuki, Yuka ^b,d   Murakami, Masahiko ^b   Izuoka, Kiyora ^b   Chang, Jie ^b,e   Wu, Wenting ^b   Yamada, Yoshiji ^b   Ichihara, Sahoko ^b  

^a SUGIYAMA JOGAKUEN UNIVERSITY   (Japan)

^b MIE UNIVERSITY   (Japan)

^c TOKYO UNIVERSITY OF SCIENCE   (Japan)

^d KYOTO UNIVERSITY   (Japan)

^e MEDICAL COLLEGE OF SOOCHOW UNIVERSITY   (China)

Author keywords

Food additive; Inflammation; Intestinal epithelium; Macrophage; Nanoparticles; Reactive oxygen species; Titanium dioxide

Indexed keywords

INTERLEUKIN 1BETA; INTERLEUKIN 8; REACTIVE OXYGEN METABOLITE; TITANIUM DIOXIDE; TITANIUM DIOXIDE NANOPARTICLE; FOOD DYE; NANOPARTICLE; TITANIUM;

ARTICLE; CACO 2 CELL LINE; CELL VIABILITY; CONTROLLED STUDY; CRYSTAL STRUCTURE; CYTOTOXICITY; FLOW CYTOMETRY; HUMAN; HUMAN CELL; INFLAMMATION; MACROPHAGE; PARTICLE SIZE; POLYMERASE CHAIN REACTION; THP 1 MACROPHAGE; CACO-2 CELL LINE; CELL LINE; CELL SURVIVAL; DRUG EFFECTS; IMMUNOLOGY; INTESTINE MUCOSA;

CACO-2 CELLS; CELL LINE; CELL SURVIVAL; FOOD COLORING AGENTS; HUMANS; INFLAMMATION; INTERLEUKIN-1BETA; INTERLEUKIN-8; INTESTINAL MUCOSA; MACROPHAGES; NANOPARTICLES; PARTICLE SIZE; REACTIVE OXYGEN SPECIES; TITANIUM;

EID: 84964329637     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms17040576     Document Type: Article

References (48)

1. Gwinn, M.R.; Vallyathan, V. Nanoparticles: Health effects—Pros and cons. Environ. Health Perspect. 2006, 114, 1818-1825. [CrossRef] [PubMed]
2. Nel, A.E.; Mädler, L.; Velegol, D.; Xia, T.; Hoek, E.M.; Somasundaran, P.; Klaessig, F.; Castranova, V.; Thompson, M. Understanding biophysicochemical interactions at the nano-bio interface. Nat. Mater. 2009, 8, 543-557. [CrossRef] [PubMed]
3. Wiesenthal, A.; Hunter, L.; Wang, S.; Wickliffe, J.; Wilkerson, M. Nanoparticles: Small and mighty. Int. J. Dermatol. 2011, 50, 247-254. [CrossRef] [PubMed]
4. Chaudhry, Q.; Scotter, M.; Blackburn, J.; Ross, B.; Boxall, A.; Castle, L.; Aitken, R.; Watkins, R. Applications and implications of nanotechnologies for the food sector. Food Addit. Contam. A Chem. Anal. Control Expo. Risk Assess. 2008, 25, 241-258. [CrossRef] [PubMed]
5. Chen, X.; Mao, S.S. Titanium dioxide nanomaterials: Synthesis, properties, modifications, and applications. Chem. Rev. 2007, 107, 2891-2959. [CrossRef] [PubMed]
6. 2 sol-gel type syntheses and its applications. J. Mater. Sci. 2011, 46, 3669-3686. [CrossRef]
7. Long, T.C.; Tajuba, J.; Sama, P.; Saleh, N.; Swartz, C.; Parker, J.; Hester, S.; Lowry, G.V.; Veronesi, B. Nanosize titanium dioxide stimulates reactive oxygen species in brain microglia and damages neurons in vitro. Environ. Health Perspect. 2007, 115, 1631-1637. [CrossRef] [PubMed]
8. 2 nanoparticles: Application to the modeling of their aggregation kinetics. J. Colloid Interface Sci. 2013, 406, 75-85. [CrossRef] [PubMed]
9. Liu, K.; Lin, X.; Zhao, J. Toxic effects of the interaction of titanium dioxide nanoparticles with chemicals or physical factors. Int. J. Nanomed. 2013, 8, 2509-2520.
10. Rashidi, L.; Khosravi-Darani, K. The applications of nanotechnology in food industry. Crit. Rev. Food Sci. Nutr. 2011, 51, 723-730. [CrossRef] [PubMed]
11. 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, 2242-2250. [CrossRef] [PubMed]
12. Chen, X.X.; Cheng, B.; Yang, Y.X.; Cao, A.; Liu, J.H.; Du, L.J.; Liu, Y.; Zhao, Y.; Wang, H. Characterization and preliminary toxicity assay of nano-titanium dioxide additive in sugar-coated chewing gum. Small 2013, 9, 1765-1774. [CrossRef] [PubMed]
13. Hussain, S.; Vanoirbeek, J.A.J.; Luyts, K.; de Vooght, V.; Verbeken, E.; Thomassen, L.C.J.; Martens, J.A.; Dinsdale, D.; Boland, S.; Marano, F.; et al. Lung exposure to nanoparticles modulates an asthmatic response in a mouse model. Eur. Respir. J. 2011, 37, 299-309. [CrossRef] [PubMed]
14. Wu, W.; Ichihara, G.; Suzuki, Y.; Izuoka, K.; Oikawa-Tada, S.; Chang, J.; Sakai, K.; Miyazawa, K.; Porter, D.; Castranova, V.; et al. Dispersion method for safety research on manufactured nanomaterials. Ind. Health 2013, 52, 54-65. [CrossRef] [PubMed]
15. Wu, W.; Ichihara, G.; Hashimoto, N.; Hasegawa, Y.; Hayashi, Y.; Tada-Oikawa, S.; Suzuki, Y.; Chang, J.; Kato, M.; D’Alessandro-Gabazza, C.N.; et al. Synergistic effect of bolus exposure to zinc oxide nanoparticles on bleomycin-induced secretion of pro-fibrotic cytokines without lasting fibrotic changes in murine lungs. Int. J. Mol. Sci. 2014, 16, 660-676. [CrossRef] [PubMed]
16. Huerta-García, E.; Pérez-Arizti, J.A.; Márquez-Ramírez, S.G.; Delgado-Buenrostro, N.L.; Chirino, Y.I.; Iglesias, G.G.; López-Marure, R. Titanium dioxide nanoparticles induce strong oxidative stress and mitochondrial damage in glial cells. Free Radic. Biol. Med. 2014, 73, 84-94. [CrossRef] [PubMed]
17. Ishimoto, Y.; Nakai, Y.; Satsu, H.; Totsuka, M.; Shimizu, M. Transient up-regulation of immunity- and apoptosis-related genes in Caco-2 cells cocultured with THP-1 cells evaluated by DNA microarray analysis. Biosci. Biotechnol. Biochem. 2010, 74, 437-439. [CrossRef] [PubMed]
18. Mastrofrancesco, A.; Alfè, M.; Rosato, E.; Gargiulo, V.; Beatrice, C.; Di Blasio, G.; Zhang, B.; Su, D.S.; Picardo, M.; Fiorito, S. Proinflammatory effects of diesel exhaust nanoparticles on scleroderma skin cells. J. Immunol. Res. 2014, 2014, 138751. [CrossRef] [PubMed]
19. Oberdörster, G.; Maynard, A.; Donaldson, K.; Castranova, V.; Fitzpatrick, J.; Ausman, K.; Carter, J.; Karn, B.; Kreyling, W.; Lai, D.; et al. Principles for characterizing the potential human health effects from exposure to nanomaterials: Elements of a screening strategy. Part. Fibre Toxicol. 2005, 2, 8. [CrossRef] [PubMed]
20. 2 rods and dots in rats: Toxicity is not dependent upon particle size and surface area. Toxicol. Sci. 2006, 91, 227-236. [CrossRef] [PubMed]
21. 2 particles: Differential responses related to surface properties. Toxicology 2007, 230, 90-104. [CrossRef] [PubMed]
22. Sayes, C.M.; Wahi, R.; Kurian, P.A.; Liu, Y.; West, J.L.; Ausman, K.D.; Warheit, D.B.; Colvin, V.L. Correlating nanoscale titania structure with toxicity: A cytotoxicity and inflammatory response study with human dermal fibroblasts and human lung epithelial cells. Toxicol. Sci. 2006, 92, 174-185. [CrossRef] [PubMed]
23. Suzuki, Y.; Tada-Oikawa, S.; Ichihara, G.; Yabata, M.; Izuoka, K.; Suzuki, M.; Sakai, K.; Ichihara, S. Zinc oxide nanoparticles induce migration and adhesion of monocytes to endothelial cells and accelerate foam cell formation. Toxicol. Appl. Pharmacol. 2014, 278, 16-25.
24. Ohtani, B.; Prieto-Mahaney, O.O.; Li, D.; Abe, R. What is Degussa (Evonik) P25? Crystalline composition analysis, reconstruction from isolated pure particles and photocatalytic activity test. J. Photochem. Photobiol. A 2010, 216, 179-182. [CrossRef]
25. Wang, J.; Zhou, G.; Chen, C.; Yu, H.; Wang, T.; Ma, Y.; Jia, G.; Gao, Y.; Li, B.; Sun, J.; et al. Acute toxicity and biodistribution of different sized titanium dioxide particles in mice after oral administration. Toxicol. Lett. 2007, 168, 176-185. [CrossRef] [PubMed]
26. 2 particles as a component of nanoparticle risk management. Toxicol. Lett. 2007, 10, 99-110. [CrossRef] [PubMed]
27. Cho, W.S.; Kang, B.C.; Lee, J.K.; Jeong, J.; Che, J.H.; Seok, S.H. Comparative absorption, distribution, and excretion of titanium dioxide and zinc oxide nanoparticles after repeated oral administration. Part. Fibre Toxicol. 2013, 10, 9. [CrossRef] [PubMed]
28. Geraets, L.; Oomen, A.G.; Krystek, P.; Jacobsen, N.R.; Wallin, H.; Laurentie, M.; Verharen, H.W.; Brandon, E.F.; de Jong, W.H. Tissue distribution and elimination after oral and intravenous administration of different titanium dioxide nanoparticles in rats. Part. Fibre Toxicol. 2014, 11, 30. [CrossRef] [PubMed]
29. 2 nanoparticles in murine dendritic cells. Nanotoxicology 2011, 5, 326-340. [CrossRef] [PubMed]
30. Yazdi, A.S.; Guarda, G.; Riteau, N.; Drexler, S.K.; Tardivel, A.; Couillin, I.; Tschopp, J. Nanoparticles activate the NLR pyrin domain containing 3 (Nlrp3) inflammasome and cause pulmonary inflammation through release of IL-1 and IL-1. Proc. Natl. Acad. Sci. USA 2010, 107, 19449-19454. [CrossRef] [PubMed]
31. Morishige, T.; Yoshioka, Y.; Tanabe, A.; Yao, X.; Tsunoda, S.; Tsutsumi, Y.; Mukai, Y.; Okada, N.; Nakagawa, S. Titanium dioxide induces different levels of IL-1 production dependent on its particle characteristics through caspase-1 activation mediated by reactive oxygen species and cathepsin B. Biochem. Biophys. Res. Commun. 2010, 392, 160-165. [CrossRef] [PubMed]
32. Xia, T.; Hamilton, R.F.; Bonner, J.C.; Crandall, E.D.; Elder, A.; Fazlollahi, F.; Girtsman, T.A.; Kim, K.; Mitra, S.; Ntim, S.A.; et al. Interlaboratory evaluation of in vitro cytotoxicity and inflammatory responses to engineered nanomaterials: The NIEHS Nano GO Consortium. Environ. Health Perspect. 2013, 121, 683-690. [CrossRef] [PubMed]
33. Van de Veerdonk, F.L.; Smeekens, S.P.; Joosten, L.A.; Kullberg, B.J.; Dinarello, C.A.; van der Meer, J.W.; Netea, M.G. Reactive oxygen species-independent activation of the IL-1 inflammasome in cells from patients with chronic granulomatous disease. Proc. Natl. Acad. Sci. USA 2010, 16, 3030-3033. [CrossRef] [PubMed]
34. Iyer, S.S.; He, Q.; Janczy, J.R.; Elliott, E.I.; Zhong, Z.; Olivier, A.K.; Sadler, J.J.; Knepper-Adrian, V.; Han, R.; Qiao, L.; et al. Mitochondrial cardiolipin is required for Nlrp3 inflammasome activation. Immunity 2013, 39, 311-323. [CrossRef] [PubMed]
35. Powell, J.J.; Faria, N.; Thomas-McKay, E.; Pele, L.C. Origin and fate of dietary nanoparticles and microparticles in the gastrointestinal tract. J. Autoimmun. 2010, 34, J226-J233. [CrossRef] [PubMed]
36. Lomer, M.C.; Thompson, R.P.; Powell, J.J. Fine and ultrafine particles of the diet: Influence on the mucosal immune response and association with Crohn’s disease. Proc. Nutr. Soc. 2002, 61, 123-130. [CrossRef] [PubMed]
37. Gerloff, K.; Pereira, D.I.; Faria, N.; Boots, A.W.; Kolling, J.; Förster, I.; Albrecht, C.; Powell, J.J.; Schins, R.P. Influence of simulated gastrointestinal conditions on particle-induced cytotoxicity and interleukin-8 regulation in differentiated and undifferentiated Caco-2 cells. Nanotoxicology 2013, 7, 353-366. [CrossRef] [PubMed]
38. Kang, T.; Guan, R.; Chen, X.; Song, Y.; Jiang, H.; Zhao, J. In vitro toxicity of different-sized ZnO nanoparticles in Caco-2 cells. Nanoscale Res. Lett. 2013, 8, 496. [CrossRef] [PubMed]
39. 2 nanoparticles: Physicochemical characterisation and toxicological effects on human colon carcinoma cells. Nanotoxicology 2013, 7, 1361-1372. [CrossRef] [PubMed]
40. Abbott Chalew, T.E.; Schwab, K.J. Toxicity of commercially available engineered nanoparticles to Caco-2 and SW480 human intestinal epithelial cells. Cell Biol. Toxicol. 2013, 29, 101-116. [CrossRef] [PubMed]
41. Courtois, A.; Andujar, P.; Ladeiro, Y.; Baudrimont, I.; Delannoy, E.; Leblais, V.; Begueret, H.; Galland, M.A.; Brochard, P.; Marano, F.; et al. Impairment of NO-dependent relaxation in intralobar pulmonary arteries: Comparison of urban particulate matter and manufactured nanoparticles. Environ. Health Perspect. 2008, 116, 1294-1299. [CrossRef] [PubMed]
42. Churg, A.; Xie, C.; Wang, X.; Vincent, R.; Wang, R.D. Air pollution particles activate NF-B on contact with airway epithelial cell surfaces. Toxicol. Appl. Pharmacol. 2005, 208, 37-45. [CrossRef] [PubMed]
43. 2 nanoparticles induce dysfunction and activation of human endothelial cells. Chem. Res. Toxicol. 2012, 25, 920-930. [CrossRef] [PubMed]
44. 2 nanoparticles in human colon carcinoma cells. Toxicol. Vit. 2015, 29, 1503-1512. [CrossRef] [PubMed]
45. Song, Z.M.; Chen, N.; Liu, J.H.; Tang, H.; Deng, X.; Xi, W.S.; Han, K.; Cao, A.; Liu, Y.; Wang, H. Biological effect of food additive titanium dioxide nanoparticles on intestine: An in vitro study. J. Appl. Toxicol. 2015, 35, 1169-1178. [CrossRef] [PubMed]
46. Janer, G.; Mas del Molino, E.; Fernández-Rosas, E.; Fernández, A.; Vázquez-Campos, S. Cell uptake and oral absorption of titanium dioxide nanoparticles. Toxicol. Lett. 2014, 228, 103-110. [CrossRef] [PubMed]
47. Brun, E.; Barreau, F.; Veronrsi, G.; Fayard, B.; Sorieul, S.; Chaneac, C.; Carapito, T.; Rabilloud, T.; Mabondzo, A.; Herlin-Boime, N.; et al. Titanium dioxide nanoparticle impact and translocation through ex vivo, in vivo and in vitro gut epithelia. Part. Fibre Toxicol. 2014, 11, 13. [CrossRef] [PubMed]
48. Tada-Oikawa, S.; Ichihara, G.; Suzuki, Y.; Izuoka, K.; Yamada, Y.; Mishima, T.; Ichihara, S. Zn(II) released from zinc oxide nano/micro particles suppresses vasculogenesis in human endothelial colony-forming cells. Toxicol. Rep. 2015, 2, 692-701. [CrossRef]