Metabolic effects of TIO2 nanoparticles, a common component of sunscreens and cosmetics, on human keratinocytes

Cell Death and Disease

Volumn 4, Issue 3, 2013, Pages

  Tucci, P ^a   Porta, G ^b   Agostini, M ^a   Dinsdale, D ^a   Iavicoli, I ^c   Cain, K ^a   Finazzi Agro A ^d   Melino, G ^a,d   Willis, A ^a  

^a UNIVERSITY OF CALABRIA   (Italy)

^b UNIVERSITY OF INSUBRIA   (Italy)

^c CATHOLIC UNIVERSITY   (Italy)

^d UNIVERSITY OF ROME TOR VERGATA   (Italy)

Author keywords

Apoptosis; Cancer; Cosmetics; Metabolism; Sunscreens; Titanium dioxide

Indexed keywords

COSMETIC; SUNSCREEN; TITANIUM DIOXIDE; NANOPARTICLE; REACTIVE OXYGEN METABOLITE; TITANIUM;

ARTICLE; CELL DEATH; CELL METABOLISM; CELL NUCLEUS; CELL ORGANELLE; CELL VIABILITY; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; CYTOTOXICITY; HUMAN; HUMAN CELL; HUMAN TISSUE; KERATINOCYTE; METABOLOMICS; MICROMORPHOLOGY; MITOCHONDRION; OXIDATIVE STRESS; PHAGOSOME; PRIORITY JOURNAL; TISSUE INJURY; WHOLE CELL; CELL CYCLE; CELL LINE; CHEMISTRY; CYTOLOGY; DRUG EFFECT; DRUG POTENTIATION; METABOLISM; TRANSPORT AT THE CELLULAR LEVEL;

BIOLOGICAL TRANSPORT; CELL CYCLE; CELL DEATH; CELL LINE; COSMETICS; HUMANS; KERATINOCYTES; METABOLIC NETWORKS AND PATHWAYS; MITOCHONDRIA; NANOPARTICLES; OXIDATIVE STRESS; PHAGOSOMES; REACTIVE OXYGEN SPECIES; SUNSCREENING AGENTS; TITANIUM;

EID: 84875895164     PISSN: None     EISSN: 20414889     Source Type: Journal    
DOI: 10.1038/cddis.2013.76     Document Type: Article

References (60)

1. Bernard BK, Osheroff MR, Hofmann A, Mennear JH. Toxicology and carcinogenesis studies of dietary titanium dioxide-coated mica in male and female Fischer 344 rats. J Toxicol Environ Health 1990; 29: 417-429.
2. Hart GA, Hesterberg TW. In vitro toxicity of respirable-size particles of diatomaceous earth and crystalline silica compared with asbestos and titanium dioxide. J Occup Environ Med 1998; 40: 29-42.
3. Gelis C, Girard S, Mavon A, Delverdier M, Paillous N, Vicendo P. Assessment of the skin photoprotective capacities of an organo-mineral broad-spectrum sunblock on two ex vivo skin models. Photodermatol Photoimmunol Photomed 2003; 19: 242-253.
4. Kang SJ, Kim BM, Lee YJ, Chung HW. Titanium dioxide nanoparticles trigger p53-mediated damage response in peripheral blood lymphocytes. Environ Mol Mutagen 2008; 49: 399-405.
5. Liu H, Ma L, Zhao J, Liu J, Yan J, Ruan J et al. Biochemical toxicity of nano-anatase TiO2 particles in mice. Biol Trace Elem Res 2009; 129: 170-180.
6. Hu R, Gong X, Duan Y, Li N, Che Y, Cui Y et al. Neurotoxicological effects and the impairment of spatial recognition memory in mice caused by exposure to TiO2 nanoparticles. Biomaterials 2010; 31: 8043-8050.
7. Iavicoli I, Leso V, Fontana L, Bergamaschi A. Toxicological effects of titanium dioxide nanoparticles: a review of in vitro mammalian studies. Eur Rev Med Pharmacol Sci 2011; 15: 481-508.
8. Wang J, Chen C, Liu Y, Jiao F, Li W, Lao F et al. Potential neurological lesion after nasal instillation of TiO2 nanoparticles in the anatase and rutile crystal phases. Toxicol Lett 2008; 183: 72-80.
9. Lam CW, James JT, McCluskey R, Hunter RL. Pulmonary toxicity of single-wall carbon nanotubes in mice 7 and 90 days after intratracheal instillation. Toxicol Sci 2004; 77: 126-134.
10. Oberdorster G, Ferin J, Gelein R, Soderholm SC, Finkelstein J. Role of the alveolar macrophage in lung injury: studies with ultrafine particles. Environ Health Perspect 1992; 97: 193-199.
11. Peters K, Unger RE, Kirkpatrick CJ, Gatti AM, Monari E. Effects of nano-scaled particles on endothelial cell function in vitro: studies on viability, proliferation and inflammation. J Mater Sci Mater Med 2004; 15: 321-325.
12. Carinci F, Volinia S, Pezzetti F, Francioso F, Tosi L, Piattelli A. Titanium-cell interaction: analysis of gene expression profiling. J Biomed Mater Res 2003; 66: 341-346.
13. Agostini M, Tucci P, Melino G. Cell death pathology: Perspective for human disease. Biochem Biophys Res Commun 2011; 414: 451-455.
14. Iavicoli I, Leso V, Bergamaschi A. Toxicological effects of titanium dioxide nanoparticles: a review of in vivo studies. J Nanomater 2012; doi:10.1155/2012/964381.
15. Kang MA, So EY, Simons AL, Spitz DR, Ouchi T. DNA damage induces reactive oxygen species generation through the H2AX-Nox1/Rac1 pathway. Cell Death Dis 2012; 3: e249.
16. Warheit DB, Webb TR, Colvin VL, Reed KL, Sayes CM. Pulmonary bioassay studies with nanoscale and fine-quartz particles in rats: Toxicity is not dependent upon particle size but on surface characteristics. Toxicol Sci 2007; 95: 270-280.
17. Baveye P, Laba M. Aggregation and toxicology of titanium dioxide nanoparticles. Environ Health Perspect 2008; 116: 152.
18. Waters KM, Masiello LM, Zangar RC, Tarasevich BJ, Karin NJ, Quesenberry RD et al. Macrophage responses to silica nanoparticles are highly conserved across particle sizes. Toxicol Sci 2009; 107: 553-569.
19. Okuda-Shimazaki J, Takaku S, Kanehira K, Sonezaki S, Taniguchi A. Effects of titanium dioxide nanoparticle aggregate size on gene expression. Int J Mol Sci 2010; 11: 2383-2392.
20. Cook CC, Kim A, Terao S, Gotoh A, Higuchi M. Consumption of oxygen: a mitochondrialgenerated progression signal of advanced cancer. Cell Death Dis 2011; 3: e258.
21. Gogna R, Madan E, Kuppusamy P, Pati U. Re-oxygenation causes hypoxic tumor regression through restoration of p53 wild-type conformation and post-translational modifications. Cell Death Dis 2012; 3: e286.
22. Kwon HJ, Ohmiya Y, Honma K-i, Honma S, Nagai T, Saito K et al. Synchronized ATP oscillations have a critical role in prechondrogenic condensation during chondrogenesis. Cell Death Dis 2012; 3: e278.
23. Plun-Favreau H, Burchell VS, Holmstrom KM, Yao Z, Deas E, Cain K et al. HtrA2 deficiency causes mitochondrial uncoupling through the F1F0-ATP synthase and consequent ATP depletion. Cell Death Dis 2012; 3: e335.
24. Nguyen D, Alavi MV, Kim KY, Kang T, Scott RT, Noh YH et al. A new vicious cycle involving glutamate excitotoxicity, oxidative stress and mitochondrial dynamics. Cell Death Dis 2011; 2: e240.
25. Tiede IM, Cook EA, Morsey B, Fox HS. Oxygen matters: tissue culture oxygen levels affect mitochondrial function and structure as well as responses to HIV viroproteins. Cell Death Dis 2011; 2: e246.
26. Fitzgerald JC, Camprubi MD, Dunn L, Wu HC, Ip NY, Kruger R et al. Phosphorylation of HtrA2 by cyclin-dependent kinase-5 is important for mitochondrial function. Cell Death Differ 2011; 19: 257-266.
27. Elanchezhian R, Palsamy P, Madson CJ, Mulhern ML, Lynch DW, Troia AM et al. Low glucose under hypoxic conditions induces unfolded protein response and produces reactive oxygen species in lens epithelial cells. Cell Death Dis 2012; 3: e301.
28. Badiola N, Penas C, Minano-Molina A, Barneda-Zahonero B, Fadó R, Sa'nchez-Opazo G et al. Induction of ER stress in response to oxygen-glucose deprivation of cortical cultures involves the activation of the PERK and IRE-1 pathways and of caspase-12. Cell Death Dis 2011; 2: e149.
29. Clarke S, Banfield K. In: Carmel R, Jacobsen DW (Eds.) Homocysteine in Health and Disease. Cambridge University Press: Cambridge, 2001. p 63.
30. Caudill MA, Wang JC, Melnyk S, Pogribny IP, Jernigan S, Collins MD et al. Intracellular S-adenosylhomocysteine concentrations predict global DNA hypomethylation in tissues of methyl-deficient cystathionine beta-synthase heterozygous mice. J Nutr 2001; 131: 2811-2818.
31. Choumenkovitch SF, Selhub J, Bagley PJ, Maeda N, Nadeau MR, Smith DE et al. In the cystathionine beta-synthase knockout mouse, elevations in total plasma homocysteine increase tissue S-adenosylhomocysteine, but responses of S-adenosylmethionine and DNA methylation are tissue specific. J Nutr 2002; 132: 2157-2160.
32. Jones PA, Takai D. The role of DNA methylation in mammalian epigenetics. Science 2001; 293: 1068-1070.
33. Pegg AE. Spermidine/spermine-N(1)-acetyltransferase: a key metabolic regulator. Am J Physiol Endocrinol Metab 2008; 294: 995-1010.
34. Ha HC, Sirisoma NS, Kuppusamy P, Zweier JL, Woster PM, Casero RA Jr. The natural polyamine spermine functions directly as a free radical scavenger. Proc Natl Acad Sci USA 1998; 95: 11140-11145.
35. Menu P, Mayor A, Zhou R, Tardivel A, Ichijo H, Mori K et al. ER stress activates the NLRP3 inflammasome via an UPR-independent pathway. Cell Death Dis 2011; 3: e261.
36. Minois N, Carmona-Gutierrez D, Bauer MA, Rockenfeller P, Eisenberg T, Brandhorst S et al. Spermidine promotes stress resistance in Drosophila melanogaster through autophagy-dependent and -independent pathways. Cell Death Dis 2012; 3: e401.
37. Milovic V, Turchanowa L. Polyamines and colon cancer. Biochem Soc Trans 2003; 31: 381-383.
38. Delage B, Luong P, Maharaj L, O'Riain C, Syed N, Crook T et al. Promoter methylation of argininosuccinate synthetase-1 sensitises lymphomas to arginine deiminase treatment, autophagy and caspase-dependent apoptosis. Cell Death Dis 2012; 3: e342.
39. Cho JH, Lee MK, Yoon KW, Lee J, Cho SG, Choi EJ. Arginine methylation-dependent regulation of ASK1 signaling by PRMT1. Cell Death Differ 2011; 19: 859-870.
40. Aflaki E, Doddapattar P, Radović B, Povoden S, Kolb D, Vujić N et al. C16 ceramide is crucial for triacylglycerol-induced apoptosis in macrophages. Cell Death Dis 2012; 3: e280.
41. Gills JJ, Zhang C, Abu-Asab MS, Castillo SS, Marceau C, LoPiccolo J et al. Ceramide mediates nanovesicle shedding and cell death in response to phosphatidylinositol ether lipid analogs and perifosine. Cell Death Dis 2012; 3: e340.
42. Allagnat F, Cunha D, Moore F, Vanderwinden JM, Eizirik DL, Cardozo AK. Mcl-1 downregulation by pro-inflammatory cytokines and palmitate is an early event contributing to b-cell apoptosis. Cell Death Differ 2011; 18: 328-337.
43. Lépine S, Allegood JC, Park M, Dent P, Milstien S, Spiegel S. Sphingosine-1-phosphate phosphohydrolase-1 regulates ER stress-induced autophagy. Cell Death Differ 2011; 18: 350-361.
44. Lalier L, Cartron PF, Olivier C, Logé C, Bougras G, Robert JM et al. Prostaglandins antagonistically control Bax activation during apoptosis. Cell Death Differ 2011; 18: 528-537.
45. Hagen N, Hans M, Hartmann D, Swandulla D, van Echten-Deckert G. Sphingosine-1- phosphate links glycosphingolipid metabolism to neurodegeneration via a calpainmediated mechanism. Cell Death Differ 2011; 18: 1356-1365.
46. Kim SY, Chun E, Lee KY. Phospholipase A2 of peroxiredoxin 6 has a critical role in tumor necrosis factor-induced apoptosis. Cell Death Differ 2011; 18: 1573-1583.
47. Merk HF, Baron JM, Neis MM, Obrigkeit DH, Karlberg AT. Skin: major target organ of allergic reactions to small molecular weight compounds. Toxicol Appl Pharmacol 2007; 224: 313-317.
48. Bulgar AD, Weeks LD, Miao Y, Yang S, Xu Y, Guo C et al. Removal of uracil by uracil DNA glycosylase limits pemetrexed cytotoxicity: overriding the limit with methoxyamine to inhibit base excision repair. Cell Death Dis 2011; 3: e252.
49. Candi E, Schmidt R, Melino G. The cornified envelope: a model of cell death in the skin. Nature Rev Mol Cell Biol 2005; 6: 328-340.
50. Rivetti di Val Cervo P, Lena AM, Nicoloso M, Rossi S, Mancini M, Zhou H et al. p63-microRNA feedback in keratinocyte senescence. Proc Natl Acad Sci USA 2012; 109: 1133-1138.
51. Notari M, Hu Y, Koch S, Lu M, Ratnayaka I, Zhong S et al. Inhibitor of apoptosis-stimulating protein of p53 (iASPP) prevents senescence and is required for epithelial stratification. Proc Natl Acad Sci USA 2011; 108: 16645-16650.
52. Vanbokhoven H, Melino G, Candi E, Declercq W. p63, a story of mice and men. J Invest Dermatol 2011; 131: 1196-1207.
53. Melino G. p63 is a suppressor of tumorigenesis and metastasis interacting with mutant p53. Cell Death Differ 2011; 18: 1487-1499.
54. Shimizu Y, Nakatsuru Y, Ichinose M, Takahashi Y, Kume H, Mimura J et al. Benzo[a]pyrene carcinogenicity is lost in mice lacking the aryl hydrocarbon receptor. Proc Natl Acad Sci USA 2000; 97: 779-782.
55. Aeby P, Sieber T, Beck H, Gerberick GF, Goebel G. Skin sensitization to p-phenylenediamine: the diverging roles of oxidation and N-acetylation for dendritic cell activation and the immune response. J Invest Dermatol 2008; 129: 99-109.
56. Weir A, Westerhoff P, Fabricius L, Hristovski K, von Goetz N. Titanium dioxide nanoparticles in food and personal care products. Envir Sci Technol 2012; 46: 2242-2250.
57. Knaapen AM, Borm PJA, Albrecht C, Schins RPF. Inhaled particles and lung cancer. Part A: mechanisms. Int J Cancer 2004; 109: 799-809.
58. Weinberg F, Hamanaka R, Wheaton WW, Weinberg S, Joseph J, Lopez M et al. Mitochondrial metabolism and ROS generation are essential for Kras-mediated tumorigenicity. Proc Natl Acad Sci USA 2010; 107: 8788-8793.
59. Onuma K, Sato Y, Ogawara S, Shirasawa N, Kobayashi M, Yoshitake J et al. Nano-scaled particles of titanium dioxide convert benign mouse fibrosarcoma cells into aggressive tumor cells. Am J Pathol 2009; 175: 2171-2183.
60. Tucci P, Agostini M, Grespi F, Markert EK, Terrinoni A, Vousden KH et al. Loss of p63 and its microRNA-205 target results in enhanced cell migration and metastasis in prostate cancer. Proc Natl Acad Sci USA 2012; 109: 15312-15317.