Archives of Toxicology

, Volume 86, Issue 4, pp 553–562 | Cite as

Toxicogenomic comparison of multi-wall carbon nanotubes (MWCNTs) and asbestos

  • Jin Sik Kim
  • Kyung Seuk Song
  • Jin Kyu Lee
  • Young C. Choi
  • In Seok Bang
  • Chang Soo Kang
  • Il Je Yu
Inorganic Compounds

Abstract

Carbon nanotubes (CNTs) have specific properties, including electrical and thermal conductivity, great strength, and rigidity, that allow them to be used in many fields. However, this increasing contact with humans and the environment is also raising health and safety concerns. Thus, research on the safety of CNTs has attracted much interest, including a comparison of the toxic effects of asbestos and carbon nanotubes, due to their physical similarity of a high aspect ratio (length/diameter). Nonetheless, there has not yet been a toxicogenomic comparison. Therefore, to examine toxicogenomic effects, the 50% growth inhibition (GI50) concentration was determined for multi-wall carbon nanotubes (MWCNTs) and asbestos (crocidolite) and found to be approximately 0.0135 and 0.066%, respectively, in the case of 24-h treatment of normal human bronchial epithelia (NHBE) cells. Using these GI50 concentrations, NHBE cells were then treated with MWCNTs and asbestos for 6 and 24 h, followed by a DNA microarray analysis. Among 31,647 genes, 1,201 and 1,252 were up-regulated by both asbestos and MWCNTs after 6 and 24 h of exposure, respectively. Meanwhile, 1,977 and 1,542 genes were down-regulated by both asbestos and MWNCTs after 6 and 24 h of exposure, respectively. In particular, the asbestos and MWCNTs both induced an over twofold up- and down-regulated expression of 12 mesothelioma-related genes and 22 lung cancer-related genes when compared with the negative control. Plus, the genes induced by the MWCNT exposure were expressed in the brain, lungs, epithelium, liver, and colon.

Keywords

Carbon nanotubes (CNTs) Toxicogenomics Multi-wall carbon nanotubes (MWCNTs) Asbestos (crocidolite) Mesothelioma Lung cancer 

Notes

Acknowledgments

This research was supported by the Nano R&D program through the National Research Foundation of Korea funded by the Korean Ministry of Education, Science and Technology (2010-0019156).

References

  1. Bianco A, Kostarelos K, Partidos CD, Prato M (2005) Biomedical applications of functionalised carbon nanotubes. Chem Commun 5:571–577CrossRefGoogle Scholar
  2. Bottini M, Bruckner S, Nika K, Bottini N, Bellucci S, Magrini A, Bergamaschi A, Mustelin T (2006) Multi-walled carbon nanotubes induce T lymphocyte apoptosis. Toxicol Lett 160:121–126PubMedCrossRefGoogle Scholar
  3. Camus M, Siemiatycki J, Meek B (1998) Nonoccupational exposure to chrysotile asbestos and the risk of lung cancer. N Engl J Med 338:1565–1571PubMedCrossRefGoogle Scholar
  4. Capek I (2009) Dispersions, novel nanomaterial sensors, nanoconjugates based on carbon nanotubes. Adv Colloid Interface Sci 150:63–89PubMedCrossRefGoogle Scholar
  5. Cheng N, Shi X, Ye J, Castranova V, Chen F, Leonard SS, Vallyathan V, Rojanasakul Y (1999) Role of transcription factor NF-[kappa]B in asbestos-induced TNF[alpha] response from macrophages. Exp Mol Pathol 66:201–210PubMedCrossRefGoogle Scholar
  6. Chou CC, Hsiao HY, Hong QS, Chen CH, Peng YW, Chen HW, Yang PC (2008) Single-walled carbon nanotubes can induce pulmonary injury in mouse model. Nano Lett 8:437–445PubMedCrossRefGoogle Scholar
  7. Chui D, Tian F, Ozkan CS, Wang MW, Gao H (2005) Effect of single wall carbon nanotubes on human HEK293 cells. Toxicol Lett 155:73–85CrossRefGoogle Scholar
  8. Coccini T, Roda E, Sarigiannis DA, Mustarelli P, Quartarone E, Profumo A, Manzo L (2010) Effects of water-soluble functionalized multi-walled carbon nanotubes examined by different cytotoxicity methods in human astrocyte D384 and lung A549 cells. Toxicology 269:41–53PubMedCrossRefGoogle Scholar
  9. Ding L, Stilwell J, Zhang T, Elboudwarej O, Jiang H, Se-legue JP, Cooke PA, Gray JW, Chen FF (2005) Molecular characterization of the cytotoxic mechanism of multiwall carbon nanotubes and nano-onions on human skin fibroblast. Nano Lett 5:2448–2464PubMedCrossRefGoogle Scholar
  10. Donaldson K, Aitken R, Tran L, Stone V, Duffin R, Forrest G, Alexander A (2006) Carbon nanotubes: a review of their properties in relation to pulmonary toxicology and workplace safety. Toxicol Sci 92:5–22PubMedCrossRefGoogle Scholar
  11. Garlepp M, Leong C (1995) Biological and immunological aspects of malignant mesothelioma. Eur Respir J 8:643–650PubMedGoogle Scholar
  12. Gooding JJ, Wibowon R, Liu JQ, Yang WR, Losic D, Orbons S, Mearns FJ, Shapter JG, Hibbert DB (2003) Protein electrochemistry using aligned carbon nanotube arrays. J Am Chem Soc 125:9006–9007PubMedCrossRefGoogle Scholar
  13. Helland A, Wick P, Koehler A, Schmid K, Som C (2007) Reviewing the environmental and human health knowledge base of carbon nanotubes. Environ Health Perspect 115:1125–1131PubMedCrossRefGoogle Scholar
  14. Hu H, Ni YC, Montana V, Haddon RC, Parpura V (2004) Chemically functionalized carbon nanotubes as substrates for neuronal growth. Nano Lett 4:507–511PubMedCrossRefGoogle Scholar
  15. Hubbard R, Venn A, Lewis S, Britton J (2000) Lung cancer and cryptogenic fibrosing alveolitis. A population-based cohort study. Am J Respir Crit Care Med 161:5–8PubMedGoogle Scholar
  16. IARC (1977) Monographs on the evaluation of carcinogenic risk to chemicals on man. Asbestos 14:1–106Google Scholar
  17. Ji SR, Liu C, Zhang B, Yang F, Xu J, Long J, Jin C, Fu DL, Ni QX, Yu XJ (2010) Carbon nanotubes in cancer diagnosis and therapy. Biochim Biophys Acta 1806:29–35PubMedGoogle Scholar
  18. Kam NWS, Liu Z, Dai HJ (2005) Functionalization of carbon nanotubes via cleavable disulfide bonds for efficient intracellular delivery of siRNA and potent gene silencing. J Am Chem Soc 127:12492–12493PubMedCrossRefGoogle Scholar
  19. Karlsson HL, Cronholm P, Gustafsson J, Möller L (2008) Copper oxide nanoparticles are highly toxic: a comparison between metal oxide nanoparticles and carbon nanotubes. Chem Res Toxicol 21:1726–1732PubMedCrossRefGoogle Scholar
  20. Kayat J, Gajbhiye V, Tekade RK, Jain NK (2010) Pulmonary toxicity of carbon nanotubes: a systematic report. Nanomedicine (Epub ahead of print)Google Scholar
  21. Kim JS, Song KS, Joo HJ, Lee JH, Yu IJ (2010) Determination of cytotoxicity attributed to multiwall carbon nanotubes (MWCNT) in normal human embryonic lung cell (WI-38) line. J Toxicol Environ Health A 73:1521–1529PubMedCrossRefGoogle Scholar
  22. Kim JS, Lee K, Lee YH, Cho HS, Kim KH, Choi KH, Lee SH, Song KS, Kang CS, Yu IJ (2011) Aspect ratio has no effect on genotoxicity of multi-wall carbon nanotubes. Arch Toxicol 85:775–786PubMedCrossRefGoogle Scholar
  23. Knaapen AM, Borm PJA, Albrecht C, Schins RPF (2004) Inhaled particles and lung cancer. Part A: mechanisms. Int J Cancer 109:799–809PubMedCrossRefGoogle Scholar
  24. Lam CW, James JT, McCluskey R, Arepalli S, Hunter RL (2006) A review of carbon nanotube toxicity and assessment of potential occupational and environmental health risks. Crit Rev Toxicol 36:189–217PubMedCrossRefGoogle Scholar
  25. Lee JY, Kim JS, An KH, Lee K, Kim DY, Bae DJ, Lee YH (2005) Electrophoretic and dynamic light scattering in evaluating dispersion and size distribution of single-walled carbon nanotubes. J Nanosci Nanotechnol 5:1045–1049PubMedCrossRefGoogle Scholar
  26. Leivonen S, Kähäri V-M (2007) Transforming growth factor-beta signaling in cancer invasion and metastasis. Int J Cancer 121:2119–2124PubMedCrossRefGoogle Scholar
  27. Lin Y, Taylor S, Li H, Fernando SKA, Qu L, Wang W, Gu L, Zhou B, Sun YP (2004) Advances towards bioapplications of carbon nanotubes. J Mater Chem 14:527–541CrossRefGoogle Scholar
  28. Lindberg HK, Falck GC, Suhonen S, Vippola M, Vanhala E, Catalán J, Savolainen K, Norppa H (2009) Genotoxicity of nanomaterials: DNA damage and micronuclei induced by carbon nanotubes and graphite nanofibres in human bronchial epithelial cells in vitro. Toxicol Lett 186:166–173PubMedCrossRefGoogle Scholar
  29. Liu Z, Sun XM, Nakayama-Ratchford N, Dai HJ (2007a) Supramolecular chemistry on water-soluble carbon nanotubes for drug loading and delivery. ACS Nano 1:50–56PubMedCrossRefGoogle Scholar
  30. Liu Z, Winters M, Holodniy M, Dai HJ (2007b) SiRNA delivery into human T cells and primary cells with carbon-nanotube transporters. Angew Chem Int Ed 46:2023–2027CrossRefGoogle Scholar
  31. Manna SK, Ramesh GT (2005) Interleukin-8 induces nuclear transcription factor-kB through TRAF6-dependent pathway. J Biol Chem 280:7010–7021PubMedCrossRefGoogle Scholar
  32. Mattson MP, Haddon RC, Rao AM (2000) Molecular functionalization of carbon nanotubes and use as substrates for neuronal growth. J Mol Neurosci 14:175–182PubMedCrossRefGoogle Scholar
  33. Maynard AD, Baron PA, Foley M, Shvedova AA, Kisin ER, Castranova V (2004) Exposure of carbon nanotube material: aerosol release during the handling of unrefined single walled carbon nanotube material. J Toxicol Environ Health A 67:87–108PubMedCrossRefGoogle Scholar
  34. McClellan RO (1994) Assessing health risks of synthetic vitreous fibers: an integrative approach. Reg Toxicol Pharmacol 20:S121–S134Google Scholar
  35. Mitchell LA, Gao J, Wal RV, Gigliotti A, Burchiel SW, McDonald JD (2007) Pulmonary and systemic immune response to inhaled multiwalled carbon nanotubes. Toxicol Sci 100:203–214PubMedCrossRefGoogle Scholar
  36. Monteiro-Riviere NA, Nemanich RJ, Inman AO, Wang YY, Riviere JE (2005) Multi-walled carbon nanotube interactions with human epidermal keratinocytes. Toxicol Lett 155:377–384PubMedCrossRefGoogle Scholar
  37. Murphy CJ (2002) Materials science: nanocubes and nanoboxes. Science 298:2139–2141PubMedCrossRefGoogle Scholar
  38. Nymark P, Wikman H, Hienonen-Kempas T, Anttila S (2008) Molecular and genetic changes in asbestos-related lung cancer. Cancer Lett 265:1–15PubMedCrossRefGoogle Scholar
  39. Peer D, Karp JM, Hong S, Farokhzad OC, Margalit R, Langer R (2007) Nanocarriers as an emerging platform for cancer therapy. Nat Nanotechnol 2:751–760PubMedCrossRefGoogle Scholar
  40. Peters K, Unger RE, Gatti AM, Monari E (2004) Effects of nano-scaled particles on endothelial cell function in vitro: studies on viability, proliferation and inflammation. J Mater Sci Mater Med 15:321–325PubMedCrossRefGoogle Scholar
  41. Pociask DA, Sime PJ, Brody AR (2004) Asbestos-derived reactive oxygen species activate TGF-[beta]1. Lab Invest 84:1013–1023PubMedCrossRefGoogle Scholar
  42. Poland CA, Duffin R, Kinloch I, Maynard A, Wallace WA, Seaton A, Stone V, Brown S, Macnee W, Donaldson K (2008) Carbon nanotubes introduced into the abdominal cavity of mice show asbestos-like pathogenicity in a pilot study. Nat Nanotechnol 3:423–428PubMedCrossRefGoogle Scholar
  43. Poma A, Di Giorgio ML (2008) Toxicogenomics to improve comprehension of the mechanisms underlying responses of in vitro and in vivo systems to nanomaterials: a review. Curr Genomics 9:571–585PubMedCrossRefGoogle Scholar
  44. Porter D, Sriram K, Wolfarth M, Jefferson A, Schwegler-Berry D, Andrew ME, Castranova V (2008) A biocompatible medium for nanoparticle dispersion. Nanotoxicology 2:144–154Google Scholar
  45. Pulskump K, Drabate S, Krug HF (2007) Carbon nanotubes show no sign of acute toxicity but induce intracellular reactive oxygen species in dependence on contaminants. Toxicol Lett 168:58–74CrossRefGoogle Scholar
  46. Reddy AR, Reddy YN, Krishna DR, Himabindu V (2010) Multi wall carbon nanotubes induce oxidative stress and cytotoxicity in human embryonic kidney (HEK293) cells. Toxicology 272:11–16PubMedCrossRefGoogle Scholar
  47. Sarkar S, Sharma C, Yog R, Periakaruppan A, JeJelowo O, Thomas R, Barrera EV, Rice-Ficth A, Wilson BL, Ramesh GT (2007) Analysis of stress responsive genes induced by single-walled carbon nanotubes in BJ Foreskin cells. J Nanosci Nanotechnol 7:584–592PubMedGoogle Scholar
  48. Schnitzler GR, Cheung CL, Hafner JH, Saurin AJ, Kingston RE, Lieber CM (2001) Direct imaging of human SWI/SNF-remodeled mono- and polynucleosomes by atomic force microscopy employing carbon nanotube tips. Mol Cell Biol 21:8504–8511PubMedCrossRefGoogle Scholar
  49. Shvedova AA, Kisin ER, Porter D, Schulte P, Kagan VE, Fadeel B, Castranova V (2009) Mechanisms of pulmonary toxicity and medical applications of carbon nanotubes: two faces of Janus? Pharmacol Ther 121:192–204PubMedCrossRefGoogle Scholar
  50. Simeonova PP (2009) Update on carbon nanotubes toxicity. Nanomedicine 4:373–375PubMedCrossRefGoogle Scholar
  51. Singh R, Pantarotto D, Lacerda L, Pastorin G, Klumpp C, Prato M, Bianco A, Kostarelos K (2006) Tissue biodistribution and blood clearance rates of intravenously administered carbon nanotube radiotracers. Proc Natl Acad Sci U. S. A. 103:3357–3362PubMedCrossRefGoogle Scholar
  52. Sinha N, Yeow JTW (2005) Carbon nanotubes for biomedical applications. IEEE Trans Nanobiosci 4:180–195CrossRefGoogle Scholar
  53. Tran CL, Hankin SM, Ross B, Aitken RJ, Jones AD, Donaldson K, Stone V, Tantra R (2008) An outline scoping study to determine whether high aspect ratio nanoparticles (HARN) should raise the same concerns as do asbestos fibres. IOM Report on Project CB0406, Edinburgh, UKGoogle Scholar
  54. Upton A, Barrett J, Becklake MR, Burdett G, Chatfield E, Davis JMG, Gamsu G, Hoel DG, Langer A, Lee RJ, Lippman M, Mossman BT, Morse R, Nicholson W, Peto J, Samet J, Wagner JC (1991) Asbestos in public and commercial buildings: a literature review and synthesis of current knowledge. Cambridge, Mass: Health Effects Institute-Asbestos ResearchGoogle Scholar
  55. Warshamana GS, Pociask DA, Sime P, Schwartz DA, Brody AR (2002) Susceptibility to asbestos-induced and transforming growth factor-{beta}1-induced fibroproliferative lung disease in two strains of mice. Am J Respir Cell Mol Biol 27:705–713PubMedGoogle Scholar
  56. Zhu L, Chang DW, Dai L, Hong Y (2007) DNA damage induced by multiwalled carbon nanotubes in mouse embryonic stem cells. Nano Lett 7:3592–3597PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Jin Sik Kim
    • 1
  • Kyung Seuk Song
    • 1
  • Jin Kyu Lee
    • 1
  • Young C. Choi
    • 2
  • In Seok Bang
    • 3
  • Chang Soo Kang
    • 4
  • Il Je Yu
    • 4
  1. 1.Korea Conformity LaboratoriesIncheonKorea
  2. 2.Hanwha NanotechIncheonKorea
  3. 3.Department of Biological Science and the Research Institute for Basic SciencesHoseo UniversityAsanKorea
  4. 4.Toxicological Research CenterHoseo UniversityAsanKorea

Personalised recommendations