Genotoxicity of short single-wall and multi-wall carbon nanotubes in human bronchial epithelial and mesothelial cells in vitro

Toxicology

Volumn 313, Issue 1, 2013, Pages 24-37

  Lindberg, Hanna K ^a   Falck, Ghita C M ^a   Singh, Rajinder ^b   Suhonen, Satu ^a   Järventaus, Hilkka ^a   Vanhala, Esa ^a   Catalán, Julia ^a,c   Farmer, Peter B ^b   Savolainen, Kai M ^a   Norppa, Hannu ^a  

^a FINNISH INSTITUTE OF OCCUPATIONAL HEALTH   (Finland)

^b UNIVERSITY OF LEICESTER   (United Kingdom)

^c UNIVERSITY OF ZARAGOZA   (Spain)

Author keywords

Bronchial cell; Chromosomal damage; DNA damage; Mesothelial cell; Multi wall carbon nanotube; Single wall carbon nanotube

Indexed keywords

MALONALDEHYDE; MULTI WALLED NANOTUBE; SINGLE WALLED NANOTUBE;

ARTICLE; BRONCHUS MUCOSA; COMET ASSAY; CONTROLLED STUDY; CYTOKINESIS; CYTOTOXICITY; DNA ADDUCT; DNA DAMAGE; DOSE RESPONSE; GENOTOXICITY; HUMAN; HUMAN CELL; IN VITRO STUDY; MESOTHELIUM CELL; MICRONUCLEUS; PRIORITY JOURNAL; TRANSMISSION ELECTRON MICROSCOPY;

BRONCHIAL CELL; CHROMOSOMAL DAMAGE; DNA DAMAGE; MESOTHELIAL CELL; MULTI-WALL CARBON NANOTUBE; SINGLE-WALL CARBON NANOTUBE;

BRONCHI; CELL LINE; COMET ASSAY; DNA ADDUCTS; DNA DAMAGE; DOSE-RESPONSE RELATIONSHIP, DRUG; EPITHELIAL CELLS; HUMANS; MICROSCOPY, ELECTRON, TRANSMISSION; MUTAGENICITY TESTS; NANOTUBES, CARBON; OXIDATION-REDUCTION; TIME FACTORS;

RODENTIA;

EID: 84885844621     PISSN: 0300483X     EISSN: 18793185     Source Type: Journal    
DOI: 10.1016/j.tox.2012.12.008     Document Type: Article

References (84)

1. 2 nanoparticles induce DNA damage towards human dermal fibroblasts in vitro. Nanotoxicology 2009, 3:161-171.
2. Asakura M., Sasaki T., Sugiyama T., Takaya M., Koda S., Nagano K., Arito H., Fukushima S. Genotoxicity and cytotoxicity of multi-wall carbon nanotubes in cultured Chinese hamster lung cells in comparison with chrysotile A fibers. J. Occup. Health 2010, 52:155-166.
3. 2, SiC nanoparticles and multi-walled carbon nanotubes exposure in several mammalian cell types: an in vitro study. J. Nanopart. Res. 2010, 12:61-73.
4. Bottini M., Bruckner S., Nika K., Bottini N., Bellucci S., Magrini A., Bergamaschi A., Mustelin T. Multi-walled carbon nanotubes induce T lymphocyte apoptosis. Toxicol. Lett. 2006, 160:121-126.
5. Catalán J., Järventaus H., Vippola M., Savolainen K., Norppa H. Induction of chromosomal aberrations by carbon nanotubes and titanium dioxide nanoparticles in human lymphocytes in vitro. Nanotoxicology 2012, 6:825-836.
6. Cavallo D., Fanizza C., Ursini C.L., Casciardi S., Paba E., Ciervo A., Fresegna A.M., Maiello R., Marcelloni A.M., Buresti G., Tombolini F., Bellucci S., Iavicoli S. Multi-walled carbon nanotubes induce cytotoxicity and genotoxicity in human lung epithelial cells. J. Appl. Toxicol. 2011, 32:454-464.
7. Cicchetti R., Divizia M., Valentini F., Argentin G. Effects of single-wall carbon nanotubes in human cells of the oral cavity: geno-cytotoxic risk. Toxicol. In Vitro 2011, 25:1811-1819.
8. Cui D., Tian F., Ozkan C.S., Wang M., Gao H. Effect of single wall carbon nanotubes on human HEK293 cells. Toxicol. Lett. 2005, 155:73-85.
9. Davoren M., Herzog E., Casey A., Cottineau B., Chambers G., Byrne H.J., Lyng F.M. In vitro toxicity evaluation of single walled carbon nanotubes on human A549 lung cells. Toxicol. In Vitro 2007, 21:438-448.
10. Di Giorgio M.L., Di Bucchianico S., Ragnelli A.M., Aimola P., Santucci S., Poma A. Effects of single and multi walled carbon nanotubes on macrophages: cyto and genotoxicity and electron microscopy. Mutat. Res. 2011, 722:20-31.
11. Di Sotto A., Chiaretti M., Carru G.A., Bellucci S., Mazzanti G. Multi-walled carbon nanotubes: lack of mutagenic activity in the bacterial reverse mutation assay. Toxicol. Lett. 2009, 184:192-197.
12. Doak S.H., Griffiths S.M., Manshian B., Singh N., Williams P.M., Brown A.P., Jenkins G.J. Confounding experimental considerations in nanogenotoxicology. Mutagenesis 2009, 24:285-293.
13. Donaldson K., Poland C.A., Schins R.P. Possible genotoxic mechanisms of nanoparticles: criteria for improved test strategies. Nanotoxicology 2010, 4:414-420.
14. Ema M., Imamura T., Suzuki H., Kobayashi N., Naya M., Nakanishi J. Evaluation of genotoxicity of multi-walled carbon nanotubes in a battery of in vitro and in vivo assays. Regul. Toxicol. Pharmacol. 2012, 63:188-195.
15. Ema, M., Imamura, T., Suzuki, H., Kobayashi, N., Naya, M., Nakanishi, J., 2012b. Genotoxicity evaluation for single-walled carbon nanotubes in a battery of in vitro and in vivo assays. J. Appl. Toxicol., Jul 5 [Epub ahead of print].
16. Fiorito S., Serafino A., Andreola F., Bernier P. Effects of fullerenes and single-wall carbon nanotubes on murine and human macrophages. Carbon 2006, 44:1100-1105.
17. Fenoglio I., Greco G., Tomatis M., Muller J., Raymundo-Piñero E., Béguin F., Fonseca A., Nagy J.B., Lison D., Fubini B. Structural defects play a major role in the acute lung toxicity of multiwall carbon nanotubes: physicochemical aspects. Chem. Res. Toxicol. 2008, 21:1690-1697.
18. Folkmann J.K., Risom L., Jacobsen N.R., Wallin H., Loft S., Moller P. Oxidatively damaged DNA in rats exposed by oral gavage to C60 fullerenes and single-walled carbon nanotubes. Environ. Health Perspect. 2009, 117:703-708.
19. Ghosh M., Chakraborty A., Bandyopadhyay M., Mukherjee A. Multi-walled carbon nanotubes (MWCNT): Induction of DNA damage in plant and mammalian cells. J. Hazard. Mater. 2011, 197:327-336.
20. Gonzalez L., Lison D., Kirsch-Volders M. Genotoxicity of engineered nanomaterials: a critical review. Nanotoxicology 2008, 2:252-273.
21. Haniu H., Saito N., Matsuda Y., Kim Y.A., Park K.C., Tsukahara T., Usui Y., Aoki K., Shimizu M., Ogihara N., Hara K., Takanashi S., Okamoto M., Ishigaki N., Nakamura K., Kato H. Effect of dispersants of multi-walled carbon nanotubes on cellular uptake and biological responses. Int. J. Nanomed. 2011, 6:3295-3307.
22. Haynes D.R., Rogers S.D., Howie D.W., Pearcy M.J., Vernon-Roberts B. Drug inhibition of the macrophage response to metal wear particles in vitro. Clin. Orthop. Relat. Res. 1996, 323:316-326.
23. Jacobsen N.R., Pojana G., White P., Moller P., Cohn C.A., Korsholm K.S., Vogel U., Marcomini A., Loft S., Wallin H. Genotoxicity, cytotoxicity, and reactive oxygen species induced by single-walled carbon nanotubes and C(60) fullerenes in the FE1-Mutatrade markMouse lung epithelial cells. Environ. Mol. Mutagen. 2008, 49:476-487.
24. Jacobsen N.R., Moller P., Jensen K.A., Vogel U., Ladefoged O., Loft S., Wallin H. Lung inflammation and genotoxicity following pulmonary exposure to nanoparticles in ApoE-/- mice. Part. Fibre Toxicol. 2009, 6:2.
25. Jia G., Wang H., Yan L., Wang X., Pei R., Yan T., Zhao Y., Guo X. Cytotoxicity of carbon nanomaterials: single-wall nanotube, multi-wall nanotube, and fullerene. Environ. Sci. Technol. 2005, 39:1378-1383.
26. Kagan V.E., Tyurina Y.Y., Tyurin V.A., Konduru N.V., Potapovich A.I., Osipov A.N., Kisin E.R., Schwegler-Berry D., Mercer R., Castranova V., Shvedova A.A. Direct and indirect effects of single walled carbon nanotubes on RAW 264.7 macrophages: role of iron. Toxicol. Lett. 2006, 165:88-100.
27. Karlsson H.L., Cronholm P., Gustafsson J., Moller L. Copper oxide nanoparticles are highly toxic: a comparison between metal oxide nanoparticles and carbon nanotubes. Chem. Res. Toxicol. 2008, 21:1726-1732.
28. Kato, T., Totsuka, Y., Ishino, K., Matsumoto, Y., Tada, Y., Nakae, D., Goto, S., Masuda, S., Ogo, S., Kawanishi, M., Yagi, T., Matsuda, T., Watanabe, M., Wakabayashi, K., 2012. Genotoxicity of multi-walled carbon nanotubes in both in vitro and in vivo assay systems. Nanotoxicology, Apr 4 [Epub ahead of print].
29. Kim J.S., Lee K., Lee Y.H., Cho H.S., Kim K.H., Choi K.H., Lee S.H., Song K.S., Kang C.S., Yu I.J. Aspect ratio has no effect on genotoxicity of multi-wall carbon nanotubes. Arch. Toxicol. 2011, 85:775-786.
30. Kim J.S., Sung J.H., Song K.S., Lee J.H., Kim S.M., Lee G.H., An K.H., Lee J.S., Shi J.H., Park J.D., Yu I.J. Persistent DNA damage measured by Comet assay of Sprague-Dawley rat lung cells after five days of inhalation exposure and 1 month post-exposure to dispersed multi-wall carbon nanotubes (MWCNTs) generated by new MWCNT aerosol generation system. Toxicol. Sci. 2012, 128:439-448.
31. Kisin E.R., Murray A.R., Keane M.J., Shi X.C., Schwegler-Berry D., Gorelik O., Arepalli S., Castranova V., Wallace W.E., Kagan V.E., Shvedova A.A. Single-walled carbon nanotubes: geno- and cytotoxic effects in lung fibroblast V79 cells. J Toxicol. Environ. Health A 2007, 70:2071-2079.
32. Lam C.W., James J.T., McCluskey R., Hunter R.L. Pulmonary toxicity of single-wall carbon nanotubes in mice 7 and 90 days after intratracheal instillation. Toxicol. Sci. 2004, 77:126-134.
33. Landsiedel R., Kapp M.D., Schulz M., Wiench K., Oesch F. Genotoxicity investigations on nanomaterials: Methods, preparation and characterization of test material, potential artifacts and limitations-Many questions, some answers. Mutat. Res. 2009, 681:241-258.
34. Li J.G., Li W.X., Xu J.Y., Cai X.Q., Liu R.L., Li Y.J., Zhao Q.F., Li Q.N. Comparative study of pathological lesions induced by multiwalled carbon nanotubes in lungs of mice by intratracheal instillation and inhalation. Environ. Toxicol. 2007, 22:415-421.
35. Li Z., Hulderman T., Salmen R., Chapman R., Leonard S.S., Young S.H., Shvedova A., Luster M.I., Simeonova P.P. Cardiovascular effects of pulmonary exposure to single-wall carbon nanotubes. Environ. Health Perspect. 2007, 115:377-382.
36. Lindberg H.K., Falck G.C., Suhonen S., Vippola M., Vanhala E., Catalán J., Savolainen K., Norppa H. Genotoxicity of nanomaterials: DNA damage and micronuclei induced by carbon nanotubes and graphite nanofibres in human bronchial epithelial cells in vitro. Toxicol. Lett. 2009, 186:166-173.
37. Linton A., Vardy J., Clarke S., van Zandwijk N. The ticking time-bomb of asbestos: its insidious role in the development of malignant mesothelioma. Crit. Rev. Oncol. Hematol. 2012, 84:200-212.
38. Manshian, B.B., Jenkins, G.J., Williams, P.M., Wright, C., Barron, A.R., Brown, A.P., Hondow, N., Dunstan, P.R., Rickman, R., Brady, K. and Doak, S.H., 2012. Single-walled carbon nanotubes: differential genotoxic potential associated with physico-chemical properties. Nanotoxicology, Jan 20 [Epub ahead of print].
39. Migliore L., Saracino D., Bonelli A., Colognato R., D'Errico M.R., Magrini A., Bergamaschi A., Bergamaschi E. Carbon nanotubes induce oxidative DNA damage in RAW 264.7 cells. Environ. Mol. Mutagen. 2010, 51:294-303.
40. Mitchell L.A., Gao J., Wal R.V., Gigliotti A., Burchiel S.W., McDonald J.D. Pulmonary and systemic immune response to inhaled multiwalled carbon nanotubes. Toxicol. Sci. 2007, 100:203-214.
41. Monteiro-Riviere N.A., Nemanich R.J., Inman A.O., Wang Y.Y., Riviere J.E. Multi-walled carbon nanotube interactions with human epidermal keratinocytes. Toxicol. Lett. 2005, 155:377-384.
42. Mouchet F., Landois P., Sarremejean E., Bernard G., Puech P., Pinelli E., Flahaut E., Gauthier L. Characterisation and in vivo ecotoxicity evaluation of double-wall carbon nanotubes in larvae of the amphibian Xenopus laevis. Aquat. Toxicol. 2008, 87:127-137.
43. Muller J., Huaux F., Moreau N., Misson P., Heilier J.F., Delos M., Arras M., Fonseca A., Nagy J.B., Lison D. Respiratory toxicity of multi-wall carbon nanotubes. Toxicol. Appl. Pharmacol. 2005, 207:221-231.
44. Muller J., Decordier I., Hoet P.H., Lombaert N., Thomassen L., Huaux F., Lison D., Kirsch-Volders M. Clastogenic and aneugenic effects of multi-wall carbon nanotubes in epithelial cells. Carcinogenesis 2008, 29:427-433.
45. Muller J., Delos M., Panin N., Rabolli V., Huaux F., Lison D. Absence of carcinogenic response to multiwall carbon nanotubes in a 2-year bioassay in the peritoneal cavity of the rat. Toxicol. Sci. 2009, 110:442-448.
46. Nagai H., Okazaki Y., Chew S.H., Misawa N., Yamashita Y., Akatsuka S., Ishihara T., Yamashita K., Yoshikawa Y., Yasui H., Jiang L., Ohara H., Takahashi T., Ichihara G., Kostarelos K., Miyata Y., Shinohara H., Toyokuni S. Diameter and rigidity of multiwalled carbon nanotubes are critical factors in mesothelial injury and carcinogenesis. Proc. Natl Acad. Sci. U. S. A. 2011, 108:E1330-E1338.
47. Nagai H., Toyokuni S. Differences and similarities between carbon nanotubes and asbestos fibers during mesothelial carcinogenesis: shedding light on fiber entry mechanism. Cancer Sci. 2012, 103:1378-1390.
48. Naya M., Kobayashi N., Mizuno K., Matsumoto K., Ema M., Nakanishi J. Evaluation of the genotoxic potential of single-wall carbon nanotubes by using a battery of in vitro and in vivo genotoxicity assays. Regul. Toxicol. Pharmacol. 2011, 61:192-198.
49. Nygaard U.C., Hansen J.S., Samuelsen M., Alberg T., Marioara C.D., Lovik M. Single-walled and multi-walled carbon nanotubes promote allergic immune responses in mice. Toxicol. Sci. 2009, 109:113-123.
50. Nygren J., Suhonen S., Norppa H., Linnainmaa K. DNA damage in bronchial epithelial and mesothelial cells with and without associated crocidolite asbestos fibers. Environ. Mol. Mutagen. 2004, 44:477-482.
51. Ogasawara Y., Umezu N., Ishii K. DNA damage in human pleural mesothelial cells induced by exposure to carbon nanotubes. Nihon Eiseigaku Zasshi. 2012, 67:76-83.
52. Pacurari M., Yin X.J., Ding M., Leonard S.S., Schwegler-Berry D., Ducatman B.S., Chirila M., Endo M., Castranova V., Vallyathan V. Oxidative and molecular interactions of multi-wall carbon nanotubes (MWCNT) in normal and malignant human mesothelial cells. Nanotoxicology 2008, 2:155-170.
53. Pacurari M., Yin X.J., Zhao J., Ding M., Leonard S.S., Schwegler-Berry D., Ducatman B.S., Sbarra D., Hoover M.D., Castranova V., Vallyathan V. Raw single-wall carbon nanotubes induce oxidative stress and activate MAPKs, AP-1, NF-kappaB, and Akt in normal and malignant human mesothelial cells. Environ. Health Perspect. 2008, 116:1211-1217.
54. Palomäki J., Karisola P., Pylkkänen L., Savolainen K., Alenius H. Engineered nanomaterials cause cytotoxicity and activation on mouse antigen presenting cells. Toxicology 2010, 267:125-131.
55. Palomäki J., Valimäki E., Sund J., Vippola M., Clausen P.A., Jensen K.A., Savolainen K., Matikainen S., Alenius H. Long, needle-like carbon nanotubes and asbestos activate the NLRP3 inflammasome through a similar mechanism. ACS Nano 2011, 5:6861-6870.
56. Papageorgiou I., Brown C., Schins R., Singh S., Newson R., Davis S., Fisher J., Ingham E., Case C.P. The effect of nano- and micron-sized particles of cobalt-chromium alloy on human fibroblasts in vitro. Biomaterials 2007, 28:2946-2958.
57. Patlolla A., Patlolla B., Tchounwou P. Evaluation of cell viability, DNA damage, and cell death in normal human dermal fibroblast cells induced by functionalized multiwalled carbon nanotube. Mol. Cell. Biochem. 2009, 338:225-232.
58. Patlolla A.K., Hussain S.M., Schlager J.J., Patlolla S., Tchounwou P.B. Comparative study of the clastogenicity of functionalized and nonfunctionalized multiwalled carbon nanotubes in bone marrow cells of Swiss-Webster mice. Environ. Toxicol. 2010, 25:608-621.
59. Pichardo S., Gutiérrez-Praena D., Puerto M., Sánchez E., Grilo A., Cameán A.M., Jos A. Oxidative stress responses to carboxylic acid functionalized single wall carbon nanotubes on the human intestinal cell line Caco-2. Toxicol. In Vitro 2012, 26:672-677.
60. Poland C.A., Duffin R., Kinloch I., Maynard A., Wallace W.A., Seaton A., Stone V., Brown S., Macnee W., Donaldson K. Carbon nanotubes introduced into the abdominal cavity of mice show asbestos-like pathogenicity in a pilot study. Nat. Nanotechnol. 2008, 3:423-428.
61. Pulskamp K., Diabate S., Krug H.F. Carbon nanotubes show no sign of acute toxicity but induce intracellular reactive oxygen species in dependence on contaminants. Toxicol. Lett. 2007, 168:58-74.
62. Ravichandran P., Baluchamy S., Gopikrishnan R., Biradar S., Ramesh V., Goornavar V., Thomas R., Wilson B.L., Jeffers R., Hall J.C., Ramesh G.T. Pulmonary biocompatibility assessment of inhaled single-wall and multiwall carbon nanotubes in BALB/c mice. J. Biol. Chem. 2011, 286:29725-29733.
63. Reddel R.R., Ke Y., Gerwin B.I., McMenamin M.G., Lechner J.F., Su R.T., Brash D.E., Park J.B., Rhim J.S., Harris C.C. Transformation of human bronchial epithelial cells by infection with SV40 or adenovirus-12 SV40 hybrid virus, or transfection via strontium phosphate coprecipitation with a plasmid containing SV40 early region genes. Cancer Res. 1988, 48:1904-1909.
64. Reddy A.R., Rao M.V., Krishna D.R., Himabindu V., Reddy Y.N. Evaluation of oxidative stress and anti-oxidant status in rat serum following exposure of carbon nanotubes. Regulat. Toxicol. Pharmacol. 2011, 59:251-257.
65. Sakamoto Y., Nakae D., Fukumori N., Tayama K., Maekawa A., Imai K., Hirose A., Nishimura T., Ohashi N., Ogata A. Induction of mesothelioma by a single intrascrotal administration of multi-wall carbon nanotube in intact male Fischer 344 rats. J. Toxicol. Sci. 2009, 34:65-76.
66. Sargent L.M., Hubbs A.F., Young S.H., Kashon M.L., Dinu C.Z., Salisbury J.L., Benkovic S.A., Lowry D.T., Murray A.R., Kisin E.R., Siegrist K.J., Battelli L., Mastovich J., Sturgeon J.L., Bunker K.L., Shvedova A.A., Reynolds S.H. Single-walled carbon nanotube-induced mitotic disruption. Mutat. Res. 2012, 745:28-37.
67. Sharma C.S., Sarkar S., Periyakaruppan A., Barr J., Wise K., Thomas R., Wilson B.L., Ramesh G.T. Single-walled carbon nanotubes induces oxidative stress in rat lung epithelial cells. J. Nanosci. Nanotechnol. 2007, 7:2466-2472.
68. Shvedova A.A., Castranova V., Kisin E.R., Schwegler-Berry D., Murray A.R., Gandelsman V.Z., Maynard A., Baron P. Exposure to carbon nanotube material: assessment of nanotube cytotoxicity using human keratinocyte cells. J. Toxicol. Environ. Health A 2003, 66:1909-1926.
69. Shvedova A.A., Kisin E.R., Mercer R., Murray A.R., Johnson V.J., Potapovich A.I., Tyurina Y.Y., Gorelik O., Arepalli S., Schwegler-Berry D., Hubbs A.F., Antonini J., Evans D.E., Ku B.K., Ramsey D., Maynard A., Kagan V.E., Castranova V., Baron P. Unusual inflammatory and fibrogenic pulmonary responses to single-walled carbon nanotubes in mice. Am. J. Physiol. Lung Cell Mol. Physiol. 2005, 289:L698-L708.
70. Shvedova A.A., Kisin E., Murray A.R., Johnson V.J., Gorelik O., Arepalli S., Hubbs A.F., Mercer R.R., Keohavong P., Sussman N., Jin J., Yin J., Stone S., Chen B.T., Deye G., Maynard A., Castranova V., Baron P.A., Kagan V.E. Inhalation vs. aspiration of single-walled carbon nanotubes in C57BL/6 mice: inflammation, fibrosis, oxidative stress, and mutagenesis. Am. J. Physiol. Lung Cell Mol. Physiol. 2008, 295:L552-L565.
71. Simon-Deckers A., Gouget B., Mayne-L'hermite M., Herlin-Boime N., Reynaud C., Carriere M. In vitro investigation of oxide nanoparticle and carbon nanotube toxicity and intracellular accumulation in A549 human pneumocytes. Toxicology 2008, 253:137-146.
72. Singh R., Leuratti C., Josyula S., Sipowicz M.A., Diwan B.A., Kasprzak K.S., Shuts H.A., Marnett L.J., Anderson L.M., Shuker D.E. Lobe-specific increases in malondialdehyde DNA adduct formation in the livers of mice following infection with Helicobacter hepaticus. Carcinogenesis 2001, 22:1281-1287.
73. Singh N., Manshian B., Jenkins G.J., Griffiths S.M., Williams P.M., Maffeis T.G., Wright C.J., Doak S.H. NanoGenotoxicology: the DNA damaging potential of engineered nanomaterials. Biomaterials 2009, 30:3891-3914.
74. Surrallés J., Xamena N., Creus A., Catalán J., Norppa H., Marcos R. Induction of micronuclei by five pyrethroid insecticides in whole-blood and isolated human lymphocyte cultures. Mutat. Res. 1995, 341:169-184.
75. Szendi K., Varga C. Lack of genotoxicity of carbon nanotubes in a pilot study. Anticancer Res. 2008, 28:349-352.
76. Takagi A., Hirose A., Nishimura T., Fukumori N., Ogata A., Ohashi N., Kitajima S., Kanno J. Induction of mesothelioma in p53+/- mouse by intraperitoneal application of multi-wall carbon nanotube. J. Toxicol. Sci. 2008, 33:105-116.
77. Takagi A., Hirose A., Futakuchi M., Tsuda H., Kanno J Dose-dependent mesothelioma induction by intraperitoneal administration of multi-wall carbon nanotubes in p53 heterozygous mice. Cancer Sci. 2012, 103:1001-1004.
78. Tyurina Y.Y., Kisin E.R., Murray A., Tyurin V.A., Kapralova V.I., Sparvero L.J., Amoscato A.A., Samhan-Arias A.K., Swedin L., Lahesmaa R., Fadeel B., Shvedova A.A., Kagan V.E. Global phospholipidomics analysis reveals selective pulmonary peroxidation profiles upon inhalation of single-walled carbon nanotubes. ACS Nano 2011, 5:7342-7353.
79. Vippola M., Falck G.C., Lindberg H.K., Suhonen S., Vanhala E., Norppa H., Savolainen K., Tossavainen A., Tuomi T. Preparation of nanoparticle dispersions for in-vitro toxicity testing. Hum. Exp. Toxicol. 2009, 28:377-385.
80. Wang J., Sun P., Bao Y., Liu J., An L. Cytotoxicity of single-walled carbon nanotubes on PC12 cells. Toxicol. In Vitro 2011, 25:242-250.
81. Wirnitzer U., Herbold B., Voetz M., Ragot J. Studies on the in vitro genotoxicity of baytubes, agglomerates of engineered multi-walled carbon-nanotubes (MWCNT). Toxicol. Lett. 2009, 186:160-165.
82. Witzmann F.A., Monteiro-Riviere N.A. Multi-walled carbon nanotube exposure alters protein expression in human keratinocytes. Nanomedicine 2006, 2:158-168.
83. Yang H., Liu C., Yang D., Zhang H., Xi Z. Comparative study of cytotoxicity, oxidative stress and genotoxicity induced by four typical nanomaterials: the role of particle size, shape and composition. J. Appl. Toxicol. 2008, 29:69-78.
84. Zhu L., Chang D.W., Dai L., Hong Y. DNA damage induced by multiwalled carbon nanotubes in mouse embryonic stem cells. Nano Lett. 2007, 7:3592-3597.