Effects of laser printer–emitted engineered nanoparticles on cytotoxicity, chemokine expression, reactive oxygen species, DNA methylation, and DNA damage: A comprehensive in vitro analysis in human small airway epithelial cells, macrophages, and lymphoblasts

Environmental Health Perspectives

Volumn 124, Issue 2, 2016, Pages 210-219

  Pirela, Sandra V ^a   Miousse, Isabelle R ^b   Lu, Xiaoyan ^a   Castranova, Vincent ^c   Thomas, Treye ^d   Qian, Yong ^e   Bello, Dhimiter ^a,f   Kobzik, Lester ^a   Koturbash, Igor ^b   Demokritou, Philip ^a  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^b UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^c WEST VIRGINIA UNIVERSITY   (United States)

^d Health Sciences Laboratory   (United States)

^e NATIONAL INSTITUTE FOR OCCUPATIONAL SAFETY AND HEALTH   (United States)

^f UNIVERSITY OF MASSACHUSETTS LOWELL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DIOXYGENASE; DNA METHYLTRANSFERASE; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 6; LACTATE DEHYDROGENASE; LASER PRINTER EMITTED ENGINEERED NANOPARTICLE; MACROPHAGE INFLAMMATORY PROTEIN 1BETA; METHYLCYTOSINE DIOXYGENASE; MONOCYTE CHEMOTACTIC PROTEIN 1; NANOPARTICLE; ORGANIC CARBON; PLATELET DERIVED GROWTH FACTOR AA; RANTES; REACTIVE OXYGEN METABOLITE; SILICON DIOXIDE; UNCLASSIFIED DRUG; CHEMOKINE; CYTOTOXIN;

ARTICLE; BIOASSAY; CELL CULTURE; CELL VIABILITY; CELLULAR MEMBRANE INTEGRITY ASSAY; COPY NUMBER VARIATION; CYTOTOXICITY; DNA DAMAGE; DNA METHYLATION; EPIGENETICS; EPITHELIUM CELL; EXPOSURE; FLUORESCENCE ANALYSIS; GENOTOXICITY; HUMAN; HUMAN CELL; IMMUNE RESPONSE; LYMPHOBLAST; MACROPHAGE; MATERIAL STATE; PARTICULATE MATTER; PHYSICAL PARAMETERS; POLYDISPERSITY INDEX; PRINTING; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; RESPIRATORY EPITHELIUM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSPOSON; ZETA POTENTIAL; CELL LINE; DRUG EFFECTS; GENETICS; LUNG; LYMPHOCYTE; METABOLISM;

CELL LINE; CHEMOKINES; CYTOTOXINS; DNA DAMAGE; DNA METHYLATION; EPITHELIAL CELLS; HUMANS; LUNG; LYMPHOCYTES; MACROPHAGES; NANOPARTICLES; PRINTING; REACTIVE OXYGEN SPECIES;

EID: 84956703868     PISSN: 00916765     EISSN: 15529924     Source Type: Journal    
DOI: 10.1289/ehp.1409582     Document Type: Article

References (73)

1. Anjilvel S, Asgharian B. 1995. A multiple-path model of particle deposition in the rat lung. Fundam Appl Toxicol 28:41-50.
2. Antonini J, Lawryk N, Murthy G, Brain J. 1999. Effect of welding fume solubility on lung macrophage viability and function in vitro. J Toxicol Environ Health A 58:343-363.
3. Antonini JM, Zeidler-Erdely PC, Young SH, Roberts JR, Erdely A. 2012. Systemic immune cell response in rats after pulmonary exposure to manganese- containing particles collected from welding aerosols. J Immunotoxicol 9:184-192.
4. Ayres FM, da Cruz AD, Steele P, Glickman BW. 2006. Low doses of gamma ionizing radiation increase hprt mutant frequencies of TK6 cells without triggering the mutator phenotype pathway. Genet Mol Biol 29:558-561.
5. Baccarelli A, Wright RO, Bollati V, Tarantini L, Litonjua AA, Suh HH, et al. 2009. Rapid DNA methylation changes after exposure to traffic particles. Am J Respir Crit Care Med 179:572-578.
6. Bai R, Zhang L, Liu Y, Meng L, Wang L, Wu Y, et al. 2010. Pulmonary responses to printer toner particles in mice after intratracheal instillation. Toxicol Lett 199:288-300.
7. Bajpayee M, Kumar A, Dhawan A. 2013. The comet assay: assessment of in vitro and in vivo DNA damage. Methods Mol Biol 1044:325-345.
8. Cohen J, Deloid G, Pyrgiotakis G, Demokritou P. 2013. Interactions of engineered nanomaterials in physiological media and implications for in vitro dosimetry. Nanotoxicology 7:417-431.
9. Cohen JM, Derk R, Wang L, Godleski J, Kobzik L, Brain J, et al. 2014a. Tracking translocation of industrially relevant engineered nanomaterials (ENMs) across alveolar epithelial monolayers in vitro. Nanotoxicology 8(suppl 1):216-225.
10. Cohen JM, Teeguarden JG, Demokritou P. 2014b. An integrated approach for the in vitro dosimetry of engineered nanomaterials. Part Fibre Toxicol 11:20; doi:10.1186/1743-8977-11-20.
11. Comar M, Zanotta N, Bonotti A, Tognon M, Negro C, Cristaudo A, et al. 2014. Increased levels of C-C chemokine RANTES in asbestos exposed workers and in malignant mesothelioma patients from an hyperendemic area. PLoS One 9:e104848; doi:10.1371/journal.pone.0104848.
12. Daigneault M, Preston JA, Marriott HM, Whyte MK, Dockrell DH. 2010. The identification of markers of macrophage differentiation in PMA-stimulated THP-1 cells and monocyte-derived macrophages. PloS One 5:e8668; doi:10.1371/journal.pone.0008668.
13. DeLoid G, Cohen JM, Darrah T, Derk R, Rojanasakul L, Pyrgiotakis G, et al. 2014. Estimating the effective density of engineered nanomaterials for in vitro dosimetry. Nat Commun 5:3514; doi:10.1038/ncomms4514.
14. Demokritou P, Büchel R, Molina RM, Deloid GM, Brain JD, Pratsinis SE. 2010. Development and characterization of a versatile engineered nanomaterial generation system (VENGES) suitable for toxicological studies. Inhal Toxicol 22(suppl 2):107-116.
15. Demokritou P, Gass S, Pyrgiotakis G, Cohen JM, Goldsmith W, McKinney W, et al. 2013. An in vivo and in vitro toxicological characterisation of realistic nanoscale CeO2 inhalation exposures. Nanotoxicology 7:1338-1350.
16. Demokritou P, Kavouras IG, Ferguson ST, Koutrakis P. 2002. Development of a high volume cascade impactor for toxicological and chemical characterization studies. Aerosol Sci Technol 36:925-933.
17. Deshmane SL, Kremlev S, Amini S, Sawaya BE. 2009. Monocyte chemoattractant protein-1 (MCP-1): an overview. J Interferon Cytokine Res 29:313-326.
18. Doak SH, Griffiths SM, Manshian B, Singh N, Williams PM, Brown AP, et al. 2009. Confounding experimental considerations in nanogenotoxicology. Mutagenesis 24:285-293.
19. Don Porto Carero A, Hoet PH, Verschaeve L, Schoeters G, Nemery B. 2001. Genotoxic effects of carbon black particles, diesel exhaust particles, and urban air particulates and their extracts on a human alveolar epithelial cell line (A549) and a human monocytic cell line (THP-1). Environ Mol Mutagen 37:155-163.
20. Dong J, Porter DW, Batteli LA, Wolfarth MG, Richardson DL, Ma Q. 2015. Pathologic and molecular profiling of rapid-onset fibrosis and inflammation induced by multi-walled carbon nanotubes. Arch Toxicol 89:621-633.
21. Ehrlich M, Lacey M. 2013. DNA hypomethylation and hemimethylation in cancer. Adv Exp Med Biol 754:31-56.
22. Fragou D, Fragou A, Kouidou S, Njau S, Kovatsi L. 2011. Epigenetic mechanisms in metal toxicity. Toxicol Mech Methods 21:343-352.
23. Fröhlich E, Samberger C, Kueznik T, Absenger M, Roblegg E, Zimmer A, et al. 2009. Cytotoxicity of nanoparticles independent from oxidative stress. J Toxicol Sci. 34:363-375.
24. Furukawa Y, Aizawa Y, Okada M, Watanabe M, Niitsuya M, Kotani M. 2002. Negative effect of photocopier toner on alveolar macrophages determined by in vitro magnetometric evaluation. Ind Health 40:214-221.
25. Gminski R, Decker K, Heinz C, Seidel A, Könczöl M, Goldenberg E, et al. 2011. Genotoxic effects of three selected black toner powders and their dimethyl sulfoxide extracts in cultured human epithelial A549 lung cells in vitro. Environ Mol Mutagen 52:296-309.
26. Gong C, Tao G, Yang L, Liu J, Liu Q, Zhuang Z. 2010. SiO2 nanoparticles induce global genomic hypomethylation in HaCaT cells. Biochem Biophys Res Commun 397:397-400.
27. Hayden PJ, Bolmarcich J, Armento A, Jackson GR Jr, Hackett TL, Knight TL, et al. 2009. Role of Toll-like receptor (TLR) activation in asthma exacerbation: experiments with in vitro models of human airway epithelial cells (EpiAirway) and epithelial cell/fibroblast co-cultures (EpiAirway-FT). In: American Thoracic Society Annual Meeting, 15-20 May 2009. San Diego, CA, 509.
28. He C, Morawska L, Taplin L. 2007. Particle emission characteristics of office printers. Environ Sci Technol 41:6039-6045.
29. He YF, Li BZ, Li Z, Liu P, Wang Y, Tang Q, et al. 2011. Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science 333:1303-1307.
30. Hillegass JM, Miller JM, MacPherson MB, Westbom CM, Sayan M, Thompson JK, et al. 2013. Asbestos and erionite prime and activate the NLRP3 inflammasome that stimulates autocrine cytokine release in human mesothelial cells. Part Fibre Toxicol 10:39; doi:10.1186/1743-8977-10-39.
31. Holder AL, Goth-Goldstein R, Lucas D, Koshland CP. 2012. Particle-induced artifacts in the MTT and LDH viability assays. Chem Res Toxicol 25:1885-1892.
32. IDC (International Data Corporation). 2014. IDC finds continued growth in the worldwide hardcopy peripherals market in the fourth quarter of 2013. Press release (Framingham, MA) 19 February. Available: http://www.idg.com/www/pr.nsf/ByID/MYAR-9GHPWU [accessed 15 December 2015].
33. Ito S, Shen L, Dai Q, Wu SC, Collins LB, Swenberg JA, et al. 2011. Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science 333:1300-1303.
34. Jin SG, Jiang Y, Qiu R, Rauch TA, Wang Y, Schackert G, et al. 2011. 5-Hydroxymethylcytosine is strongly depleted in human cancers but its levels do not correlate with IDH1 mutations. Cancer Res 71:7360-7365.
35. Jones PA. 2012. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet 13:484-492.
36. Khatri M, Bello D, Gaines P, Martin J, Pal AK, Gore R, et al. 2013a. Nanoparticles from photocopiers induce oxidative stress and upper respiratory tract inflammation in healthy volunteers. Nanotoxicology 7:1014-1027.
37. Khatri M, Bello D, Pal AK, Cohen JM, Woskie S, Gassert T, et al. 2013b. Evaluation of cytotoxic, genotoxic and inflammatory responses of nanoparticles from photocopiers in three human cell lines. Part Fibre Toxicol 10:42; doi:10.1186/1743-8977-10-42.
38. Kimura A, Miyata A, Honma M. 2013. A combination of in vitro comet assay and micronucleus test using human lymphoblastoid TK6 cells. Mutagenesis 28:583-590.
39. Koturbash I, Scherhag A, Sorrentino J, Sexton K, Bodnar W, Tryndyak V, et al. 2011. Epigenetic alterations in liver of C57BL/6J mice after short- term inhalational exposure to 1,3-butadiene. Environ Health Perspect 119:635-640; doi:10.1289/ehp.1002910.
40. Koturbash I, Simpson NE, Beland FA, Pogribny IP. 2012. Alterations in histone H4 lysine 20 methylation: implications for cancer detection and prevention. Antioxid Redox Signal 17:365-374.
41. L’Azou B, Jorly J, On D, Sellier E, Moisan F, Fleury-Feith J, et al. 2008. In vitro effects of nanoparticles on renal cells. Part Fibre Toxicol 5:22; doi:10.1186/1743-8977-5-22.
42. Lacy P, Stow JL. 2011. Cytokine release from innate immune cells: association with diverse membrane trafficking pathways. Blood 118:9-18.
43. Li Z, Cai X, Cai CL, Wang J, Zhang W, Petersen BE, et al. 2011. Deletion of Tet2 in mice leads to dysregulated hematopoietic stem cells and subsequent development of myeloid malignancies. Blood 118:4509-4518.
44. Liu JY, Hu JH, Zhu QG, Li FQ, Wang J, Sun HJ. 2007. Effect of matrine on the expression of substance P receptor and inflammatory cytokines production in human skin keratinocytes and fibroblasts. Int Immunopharmacol 7:816-823.
45. Lu X, Miousse IR, Pirela SV, Melnyk S, Koturbash I, Demokritou P. 2015. Short-term exposure to engineered nanomaterials affects cellular epigenome. Nanotoxicology; doi:10.3109/17435390.2015.1025115 [Online 4 May 2015].
46. Madrigano J, Baccarelli A, Mittleman MA, Wright RO, Sparrow D, Vokonas PS, et al. 2011. Prolonged exposure to particulate pollution, genes associated with glutathione pathways, and DNA methylation in a cohort of older men. Environ Health Perspect 119:977-982; doi:10.1289/ehp.1002773.
47. Miousse IR, Chalbot MC, Aykin-Burns N, Wang X, Basnakian A, Kavouras IG, et al. 2014a. Epigenetic alterations induced by ambient particulate matter in mouse macrophages. Environ Mol Mutagen 55:428-435.
48. Miousse IR, Chalbot MC, Lumen A, Ferguson A, Kavouras IG, Koturbash I. 2015. Response of transposable elements to environmental stressors. Mutat Res Rev Mutat Res 765:19-39.
49. Miousse IR, Shao L, Chang J, Feng W, Wang Y, Allen AR, et al. 2014b. Exposure to low dose 56Fe-ion radiation induces long-term epigenetic alterations in mouse bone marrow hematopoietic progenitor and stem cells. Radiat Res 182:92-101.
50. Mittal S, Pandey AK. 2014. Cerium oxide nanoparticles induced toxicity in human lung cells: role of ROS mediated DNA damage and apoptosis. BioMed Res Int 2014:891934; doi:10.1155/2014/891934.
51. Monteiro-Riviere NA, Inman AO, Zhang LW. 2009. Limitations and relative utility of screening assays to assess engineered nanoparticle toxicity in a human cell line. Toxicol Appl Pharmacol 234:222-235.
52. Morawska L, He C, Johnson G, Jayaratne R, Salthammer T, Wang H, et al. 2009. An investigation into the characteristics and formation mechanisms of particles originating from the operation of laser printers. Environ Sci Technol 43:1015-1022.
53. Morimoto Y, Oyabu T, Horie M, Kambara T, Izumi H, Kuroda E, et al. 2013. Pulmonary toxicity of printer toner following inhalation and intratracheal instillation. Inhal Toxicol 25:679-690.
54. Nyga A, Hart A, Tetley TD. 2015. Importance of the HIF pathway in cobalt nanoparticle-induced cytotoxicity and inflammation in human macrophages. Nanotoxicology 9:905-917.
55. Pal AK, Bello D, Cohen J, Demokritou P. 2015. Implications of in vitro dosimetry on toxicological ranking of low aspect ratio engineered nanomaterials. Nanotoxicology 9:871-185.
56. Pirela S, Molina R, Watson C, Cohen JM, Bello D, Demokritou P, et al. 2013. Effects of copy center particles on the lungs: a toxicological characterization using a Balb/c mouse model. Inhal Toxicol 25:498-508.
57. Pirela SV, Pyrgiotakis G, Bello D, Thomas T, Castranova V, Demokritou P. 2014. Development and characterization of an exposure platform suitable for physico-chemical, morphological and toxicological characterization of printer-emitted particles (PEPs). Inhal Toxicol 26:400-408.
58. Pirela SV, Sotiriou GA, Bello D, Shafer M, Bunker KL, Castranova V, et al. 2015. Consumer exposures to laser printer-emitted engineered nanoparticles: a case study of life-cycle implications from nanoenabled products. Nanotoxicology 9:760-768.
59. Ritter M, Mennerich D, Weith A, Seither P. 2005. Characterization of Toll-like receptors in primary lung epithelial cells: strong impact of the TLR3ligand poly(I:C) on the regulation of Toll-like receptors,adaptor proteins and inflammatory response. J Inflamm (Lond) 2:16; doi:10.1186/1476-9255-2-16.
60. Rudin CM, Thompson CB. 2001. Transcriptional activation of short interspersed elements by DNA-damaging agents. Genes Chromosomes Cancer 30:64-71.
61. Setyawati MI, Tay CY, Chia SL, Goh SL, Fang W, Neo MJ, et al. 2013. Titanium dioxide nanomaterials cause endothelial cell leakiness by disrupting the homophilic interaction of VE-cadherin. Nat Commun 4:1673; doi:10.1038/ncomms2655.
62. Sisler JD, Pirela SV, Friend S, Farcas M, Schwegler-Berry D, Shvedova A, et al. 2015. Small airway epithelial cells exposure to printer-emitted engineered nanoparticles induces cellular effects on human microvascular endothelial cells in an alveolar-capillary co-culture model. Nanotoxicology 9:769-779.
63. Smith ZD, Chan MM, Mikkelsen TS, Gu H, Gnirke A, Regev A, et al. 2012. A unique regulatory phase of DNA methylation in the early mammalian embryo. Nature 484:339-344.
64. Sotiriou GA, Diaz E, Long MS, Godleski J, Brain J, Pratsinis SE, et al. 2012. A novel platform for pulmonary and cardiovascular toxicological characterization of inhaled engineered nanomaterials. Nanotoxicology 6:680-690.
65. Sriram K, Lin GX, Jefferson AM, Roberts JR, Andrews RN, Kashon ML, et al. 2012. Manganese accumulation in nail clippings as a biomarker of welding fume exposure and neurotoxicity. Toxicology 291:73-82.
66. Tang T, Gminski R, Könczöl M, Modest C, Armbruster B, Mersch-Sundermann V. 2012. Investigations on cytotoxic and genotoxic effects of laser printer emissions in human epithelial A549 lung cells using an air/liquid exposure system. Environ Mol Mutagen 53:125-135.
67. Terasaki N, Goodier JL, Cheung LE, Wang YJ, Kajikawa M, Kazazian HH, et al. 2013. In vitro screening for compounds that enhance human L1 mobilization. PloS One 8:e74629; doi:10.1371/journal.pone.0074629.
68. Wan R, Mo Y, Feng L, Chien S, Tollerud DJ, Zhang Q. 2012. DNA damage caused by metal nanoparticles: involvement of oxidative stress and activation of ATM. Chem Res Toxicol 25:1402-1411.
69. Wang H, He C, Morawska L, McGarry P, Johnson G. 2012. Ozone-initiated particle formation, particle aging, and precursors in a laser printer. Environ Sci Technol 46:704-712.
70. Watson C, Ge J, Cohen J, Pyrgiotakis G, Engelward BP, Demokritou P. 2014. High-throughput screening platform for engineered nanoparticle-mediated genotoxicity using CometChip technology. ACS Nano 8:2118-2133.
71. Wilhelmi V, Fischer U, Weighardt H, Schulze-Osthoff K, Nickel C, Stahlmecke B, et al. 2013. Zinc oxide nanoparticles induce necrosis and apoptosis in macrophages in a p47phox- and Nrf2-independent manner. PloS One 8:e65704; doi:10.1371/journal.pone.0065704.
72. Zarogiannis SG, Filippidis AS, Fernandez S, Jurkuvenaite A, Ambalavanan N, Stanishevsky A, et al. 2013. Nano-TiO2 particles impair adhesion of airway epithelial cells to fibronectin. Respir Physiol Neurobiol 185:454-460.
73. Zeidler-Erdely PC, Battelli LA, Salmen-Muniz R, Li Z, Erdely A, Kashon ML, et al. 2011. Lung tumor production and tissue metal distribution after exposure to manual metal ARC-stainless steel welding fume in A/J and C57BL/6J mice. J Toxicol Environ Health A 74:728-736.