Sonicated and stirred copper oxide nanoparticles induce similar toxicity and pro-inflammatory response in N-hTERT keratinocytes and SZ95 sebocytes

Journal of Nanoparticle Research

Volumn 16, Issue 4, 2014, Pages

  Piret, Jean Pascal ^a   Mejia, Jorge ^a   Lucas, Stéphane ^a   Zouboulis, Christos C ^b   Saout, Christelle ^a   Toussaint, Olivier ^a  

^a University of Namur   (Belgium)

^b DESSAU MEDICAL CENTER   (Germany)

Author keywords

Copper oxide nanoparticles; Inflammatory response; Keratinocytes; Sebocytes; Sonication; Toxicity

Indexed keywords

NANOPARTICLES; PEPTIDES; SONICATION; TOXICITY;

CELLULAR TOXICITIES; COPPER OXIDE NANOPARTICLES; DNA BINDING ACTIVITY; INFLAMMATORY RESPONSE; KERATINOCYTES; REACTIVE OXYGEN SPECIES; REDOX SENSITIVES; SEBOCYTES;

COPPER OXIDES;

COPPER OXIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1ALPHA; INTERLEUKIN 8; NANOPARTICLE; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR NRF2;

ARTICLE; CONTROLLED STUDY; CYTOTOXICITY; DNA BINDING; EPIDERMIS; HUMAN; HUMAN CELL; HUMAN TISSUE; INFLAMMATION; KERATINOCYTE; OXIDATION; OXIDATIVE STRESS; PARTICLE SIZE; PRIORITY JOURNAL; TRANSCRIPTOMICS; ULTRASOUND;

EID: 84896544625     PISSN: 13880764     EISSN: 1572896X     Source Type: Journal    
DOI: 10.1007/s11051-014-2337-y     Document Type: Article

References (49)

1. Alam J, Stewart D, Touchard C, Boinapally S, Choi AM, Cook JL (1999) Nrf2, a Cap'n'Collar transcription factor, regulates induction of the heme oxygenase-1 gene. J Biol Chem 274(37):26071-26078
2. Bertrand-Vallery V, Belot N, Dieu M, Delaive E, Ninane N, Demazy C, Raes M, Salmon M, Poumay Y, Debacq-Chainiaux F, Toussaint O (2010a) Proteomic profiling of human keratinocytes undergoing UVB-induced alternative differentiation reveals TRIpartite Motif Protein 29 as a survival factor. PLoS One 5(5):e10462
3. Bertrand-Vallery V, Boilan E, Ninane N, Demazy C, Friguet B, Toussaint O, Poumay Y, Debacq-Chainiaux F (2010b) Repeated exposures to UVB induce differentiation rather than senescence of human keratinocytes lacking p16(INK-4A). Biogerontology 11(2):167-181
4. Bihari P, Vippola M, Schultes S, Praetner M, Khandoga AG, Reichel CA, Coester C, Tuomi T, Rehberg M, Krombach F (2008) Optimized dispersion of nanoparticles for biological in vitro and in vivo studies. Part Fibre Toxicol 5:14
5. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248-254
6. Brasier AR (2010) The nuclear factor-kappaB-interleukin-6 signalling pathway mediating vascular inflammation. Cardiovasc Res 86(2):211-218
7. Briviba K, Klotz LO, Sies H (1997) Toxic and signaling effects of photochemically or chemically generated singlet oxygen in biological systems. Biol Chem 378(11):1259-1265 (Pubitemid 27507541)
8. Brown DM, Donaldson K, Stone V (2010) Nuclear translocation of Nrf2 and expression of antioxidant defence genes in THP-1 cells exposed to carbon nanotubes. J Biomed Nanotechnol 6(3):224-233
9. Cioffi N, Ditaranto N, Torsi L, Picca RA, Sabbatini L, Valentini A, Novello L, Tantillo G, Bleve-Zacheo T, Zambonin PG (2005) Analytical characterization of bioactive fluoropolymer ultra-thin coatings modified by copper nanoparticles. Anal Bioanal Chem 381(3):607-616 (Pubitemid 40379331)
10. Cohen D, Soroka Y, Ma'or Z, Oron M, Portugal-Cohen M, Bregegere FM, Berhanu D, Valsami-Jones E, Hai N, Milner Y (2012) Evaluation of topically applied copper(II) oxide nanoparticle cytotoxicity in human skin organ culture. Toxicol In Vitro 27(1):292-298. doi:10.1016/j.tiv.2012.08.026
11. Coquette A, Berna N, Vandenbosch A, Rosdy M, De Wever B, Poumay Y (2003) Analysis of interleukin-1alpha (IL-1alpha) and interleukin-8 (IL-8) expression and release in in vitro reconstructed human epidermis for the prediction of in vivo skin irritation and/or sensitization. Toxicol In Vitro 17(3):311-321 (Pubitemid 36627750)
12. Cronholm P, Midander K, Karlsson HL, Elihn K, Wallinder IO, Moller L (2011) Effect of sonication and serum proteins on copper release from copper nanoparticles and the toxicity towards lung epithelial cells. Nanotoxicology 5(2):269-281
13. Di Bucchianico S, Fabbrizi MR, Misra SK, Valsami-Jones E, Berhanu D, Reip P, Bergamaschi E, Migliore L (2013) Multiple cytotoxic and genotoxic effects induced in vitro by differently shaped copper oxide nanomaterials. Mutagenesis 28(3):287-299
14. Dickson MA, Hahn WC, Ino Y, Ronfard V, Wu JY, Weinberg RA, Louis DN, Li FP, Rheinwald JG (2000) Human keratinocytes that express hTERT and also bypass a p16(INK4a)-enforced mechanism that limits life span become immortal yet retain normal growth and differentiation characteristics. Mol Cell Biol 20(4):1436-1447 (Pubitemid 30069263)
15. Fahmy B, Cormier SA (2009) Copper oxide nanoparticles induce oxidative stress and cytotoxicity in airway epithelial cells. Toxicol In Vitro 23(7):1365-1371
16. Gabbay G, Borkow G, Mishal J, Magen E, Zatcoff R, Shemer-Avni Y (2006) Copper oxide impregnated textiles with potent biocidal activities. J Ind Textiles 35:323-335
17. Hanagata N, Zhuang F, Connolly S, Li J, Ogawa N, Xu M (2011) Molecular responses of human lung epithelial cells to the toxicity of copper oxide nanoparticles inferred from whole genome expression analysis. ACS Nano 5(12):9326-9338
18. 2 to bacteria Vibrio fischeri and crustaceans Daphnia magna and Thamnocephalus platyurus. Chemosphere 71(7):1308-1316
19. Kang KW, Lee SJ, Kim SG (2005) Molecular mechanism of nrf2 activation by oxidative stress. Antioxid Redox Signal 7(11-12):1664-1673 (Pubitemid 41768000)
20. Kang SJ, Ryoo IG, Lee YJ, Kwak MK (2012) Role of the Nrf2-heme oxygenase-1 pathway in silver nanoparticle-mediated cytotoxicity. Toxicol Appl Pharmacol 258(1):89-98
21. Karlsson HL, Cronholm P, Gustafsson J, Moller L (2008) Copper oxide nanoparticles are highly toxic: a comparison between metal oxide nanoparticles and carbon nanotubes. Chem Res Toxicol 21(9):1726-1732
22. Karlsson HL, Gustafsson J, Cronholm P, Moller L (2009) Size-dependent toxicity of metal oxide particles - a comparison between nano- and micrometer size. Toxicol Lett 188(2):112-118
23. 2 to yeast Saccharomyces cerevisiae. Toxicol In Vitro 23(6):1116-1122
24. Kunsch C, Rosen CA (1993) NF-kappa B subunit-specific regulation of the interleukin-8 promoter. Mol Cell Biol 13(10):6137-6146 (Pubitemid 23292608)
25. Lewis DA, Yi Q, Travers JB, Spandau DF (2008) UVB-induced senescence in human keratinocytes requires a functional insulin-like growth factor-1 receptor and p53. Mol Biol Cell 19(4):1346-1353 (Pubitemid 351805090)
26. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25(4):402-408 (Pubitemid 34164012)
27. Ma Q (2009) Transcriptional responses to oxidative stress: pathological and toxicological implications. Pharmacol Ther 125(3):376-393
28. Mejia J, Tichelaar F, Saout S, Toussaint O, Masereel B, Mekhalif Z, Lucas S, Delhalle J (2011) Effects of the dispersion methods in Pluronic F108 on the size and the surface composition of MWCNTs and their implications in toxicology assessment. J Nanopart Res 13(2):655-667
29. Midander K, Cronholm P, Karlsson HL, Elihn K, Moller L, Leygraf C, Wallinder IO (2009) Surface characteristics, copper release, and toxicity of nano- and micrometer-sized copper and copper(II) oxide particles: a cross-disciplinary study. Small 5(3):389-399
30. Mortimer M, Kasemets K, Kahru A (2009) Toxicity of ZnO and CuO nanoparticles to ciliated protozoa Tetrahymena thermophila. Toxicology 269(2-3):182-189
31. Mroz RM, Schins RP, Li H, Drost EM, Macnee W, Donaldson K (2007) Nanoparticle carbon black driven DNA damage induces growth arrest and AP-1 and NFkappaB DNA binding in lung epithelial A549 cell line. J Physiol Pharmacol 58 Suppl 5(Pt 2):461-470 (Pubitemid 351346695)
32. Nguyen T, Nioi P, Pickett CB (2009) The Nrf2-antioxidant response element signaling pathway and its activation by oxidative stress. J Biol Chem 284(20):13291-13295
33. Oberdorster G, Maynard A, Donaldson K, Castranova V, Fitzpatrick J, Ausman K, Carter J, Karn B, Kreyling W, Lai D, Olin S, Monteiro-Riviere N, Warheit D, Yang H (2005) Principles for characterizing the potential human health effects from exposure to nanomaterials: elements of a screening strategy. Part Fibre Toxicol 2:8
34. Piret J-P, Detriche S, Vigneron R, Vankoningsloo S, Rolin S, Mejia Mendoza JH, Masereel B, Lucas S, Delhalle J, Luizi F, Saout C, Toussaint O (2010) Dispersion of multi-walled carbon nanotubes in biocompatible dispersants. J Nanopart Res 12:75-82
35. Piret JP, Jacques D, Audinot JN, Mejia J, Boilan E, Noel F, Fransolet M, Demazy C, Lucas S, Saout C, Toussaint O (2012a) Copper (II) oxide nanoparticles penetrate into HepG2 cells, exert cytotoxicity via oxidative stress and induce pro-inflammatory response. Nanoscale 4:7168-7184
36. Piret JP, Vankoningsloo S, Mejia J, Noel F, Boilan E, Lambinon F, Zouboulis CC, Masereel B, Lucas S, Saout C, Toussaint O (2012b) Differential toxicity of copper (II) oxide nanoparticles of similar hydrodynamic diameter on human differentiated intestinal Caco-2 cell monolayers is correlated in part to copper release and shape. Nanotoxicology 6(7):789-803
37. Ren G, Hu D, Cheng EW, Vargas-Reus MA, Reip P, Allaker RP (2009) Characterisation of copper oxide nanoparticles for antimicrobial applications. Int J Antimicrob Agents 33(6):587-590
38. Satih S, Savinel H, Rabiau N, Fontana L, Bignon YJ, Bernard-Gallon DJ (2009) Expression analyses of nuclear receptor genes in breast cancer cell lines exposed to soy phytoestrogens after BRCA2 knockdown by TaqMan Low-Density Array (TLDA). J Mol Signal 4:3
39. Schramm A, Vandesompele J, Schulte JH, Dreesmann S, Kaderali L, Brors B, Eils R, Speleman F, Eggert A (2007) Translating expression profiling into a clinically feasible test to predict neuroblastoma outcome. Clin Cancer Res 13(5):1459-1465 (Pubitemid 46453756)
40. Singh N, Manshian B, Jenkins GJ, Griffiths SM, Williams PM, Maffeis TG, Wright CJ, Doak SH (2009) NanoGenotoxicology: the DNA damaging potential of engineered nanomaterials. Biomaterials 30(23-24):3891-3914
41. Sun Q, Tan D, Zhou Q, Liu X, Cheng Z, Liu G, Zhu M, Sang X, Gui S, Cheng J, Hu R, Tang M, Hong F (2012) Oxidative damage of lung and its protective mechanism in mice caused by long-term exposure to titanium dioxide nanoparticles. J Biomed Mater Res A 100(10):2554-2562
42. Uruno A, Motohashi H (2011) The Keap1-Nrf2 system as an in vivo sensor for electrophiles. Nitric Oxide 25(2):153-160
43. Vallyathan V, Shi X (1997) The role of oxygen free radicals in occupational and environmental lung diseases. Environ Health Perspect 105(Suppl 1):165-177 (Pubitemid 27168292)
44. Vankoningsloo S, De Pauw A, Houbion A, Tejerina S, Demazy C, de Longueville F, Bertholet V, Renard P, Remacle J, Holvoet P, Raes M, Arnould T (2006) CREB activation induced by mitochondrial dysfunction triggers triglyceride accumulation in 3T3-L1 preadipocytes. J Cell Sci 119(Pt 7):1266-1282
45. Vankoningsloo S, Piret JP, Saout C, Noel F, Mejia J, Zouboulis CC, Delhalle J, Lucas S, Toussaint O (2010) Cytotoxicity of multi-walled carbon nanotubes in three skin cellular models: effects of sonication, dispersive agents and corneous layer of reconstructed epidermis. Nanotoxicology 4(1):84-97
46. Vankoningsloo S, Piret JP, Saout C, Noel F, Mejia J, Coquette A, Zouboulis CC, Delhalle J, Lucas S, Toussaint O (2012) Pro-inflammatory effects of different MWCNTs dispersions in p16(INK4A)-deficient telomerase-expressing human keratinocytes but not in human SV-40 immortalized sebocytes. Nanotoxicology 6(1):77-93
47. Wang F, Yu L, Monopoli MP, Sandin P, Mahon E, Salvati A, Dawson KA (2013) The biomolecular corona is retained during nanoparticle uptake and protects the cells from the damage induced by cationic nanoparticles until degraded in the lysosomes. Nanomedicine 9(8):1159-1168
48. Zhou K, Wang R, Xu B, Li Y (2006) Synthesis, characterization and catalytic properties of CuO nanoparticles with various shapes. Nanotechnology 17:3939-3943 (Pubitemid 44424439)
49. Zouboulis CC, Seltmann H, Neitzel H, Orfanos CE (1999) Establishment and characterization of an immortalized human sebaceous gland cell line (SZ95). J Invest Dermatol 113(6):1011-1020 (Pubitemid 30013346)