Toxicity of single-walled carbon nanotubes

Archives of Toxicology

Volumn 90, Issue 1, 2016, Pages 103-118

  Ong, Li Chu ^a   Chung, Felicia Fei Lei ^a   Tan, Yuen Fen ^a   Leong, Chee Onn ^a  

^a INTERNATIONAL MEDICAL UNIVERSITY   (Malaysia)

Author keywords

Carbon nanotube; Nanomaterials; Nanotoxicity; Single walled; Toxicology

Indexed keywords

SINGLE WALLED NANOTUBE; CARBON NANOTUBE;

CELL TRANSPORT; CYTOTOXICITY; EXOCYTOSIS; GASTROINTESTINAL TOXICITY; NONHUMAN; PRIORITY JOURNAL; REVIEW; TISSUE DISTRIBUTION; TOXICITY; TOXICOKINETICS; ADVERSE EFFECTS; ANIMAL; ANTIBODY SPECIFICITY; BODY BURDEN; ENVIRONMENTAL EXPOSURE; HUMAN; NANOTECHNOLOGY; PHARMACOKINETICS; PROCEDURES; RISK ASSESSMENT; TOXICITY TESTING;

ANIMALS; BODY BURDEN; ENVIRONMENTAL EXPOSURE; HUMANS; NANOTECHNOLOGY; NANOTUBES, CARBON; ORGAN SPECIFICITY; PHARMACOKINETICS; RISK ASSESSMENT; TISSUE DISTRIBUTION; TOXICITY TESTS;

EID: 84955407371     PISSN: 03405761     EISSN: 14320738     Source Type: Journal    
DOI: 10.1007/s00204-014-1376-6     Document Type: Review

References (92)

1. Aggarwal P, Hall JB, McLeland CB, Dobrovolskaia MA, McNeil SE (2009) Nanoparticle interaction with plasma proteins as it relates to particle biodistribution, biocompatibility and therapeutic efficacy. Adv Drug Deliv Rev 61(6):428–437. doi:10.1016/j.addr.2009.03.009
2. Avouris P, Chen Z, Perebeinos V (2007) Carbon-based electronics. Nat Nanotechnol 2(10):605–615. doi:10.1038/nnano.2007.300
3. Azeredo H (2009) Nanocomposites for food packaging applications. Food Res Int 42(9):1240–1253
4. Bang JJ, Guerrero PA, Lopez DA, Murr LE, Esquivel EV (2004) Carbon nanotubes and other fullerene nanocrystals in domestic propane and natural gas combustion streams. J Nanosci Nanotechnol 4(7):716–718
5. Bhabra G, Sood A, Fisher B et al (2009) Nanoparticles can cause DNA damage across a cellular barrier. Nat Nanotechnol 4(12):876–883. doi:10.1038/nnano.2009.313
6. Casals E, Vázquez-Campos S, Bastús NG, Puntes V (2008) Distribution and potential toxicity of engineered inorganic nanoparticles and carbon nanostructures in biological systems. Trends Anal Chem 27(8):672–683
7. Casey A, Herzog E, Davoren M, Lyng F, Byrne H, Chambers G (2007) Spectroscopic analysis confirms the interactions between single walled carbon nanotubes and various dyes commonly used to assess cytotoxicity. Carbon 45(7):1425–1432
8. Cheng J, Fernando KA, Veca LM et al (2008) Reversible accumulation of PEGylated single-walled carbon nanotubes in the mammalian nucleus. ACS Nano 2(10):2085–2094. doi:10.1021/nn800461u
9. Cherukuri P, Bachilo SM, Litovsky SH, Weisman RB (2004) Near-infrared fluorescence microscopy of single-walled carbon nanotubes in phagocytic cells. J Am Chem Soc 126(48):15638–15639. doi:10.1021/ja0466311
10. Cherukuri P, Gannon CJ, Leeuw TK et al (2006) Mammalian pharmacokinetics of carbon nanotubes using intrinsic near-infrared fluorescence. Proc Natl Acad Sci USA 103(50):18882–18886. doi:10.1073/pnas.0609265103
11. Cicchetti R, Divizia M, Valentini F, Argentin G (2011) Effects of single-wall carbon nanotubes in human cells of the oral cavity: geno-cytotoxic risk. Toxicol In Vitro 25(8):1811–1819. doi:10.1016/j.tiv.2011.09.017
12. Coleman JN, Fleming A, Maier S et al (2004) Binding kinetics and SWNT bundle dissociation in low concentration polymer-nanotube dispersions. J Phys Chem B 108(11):3446–3450
13. Cui D, Tian F, Ozkan CS, Wang M, Gao H (2005) Effect of single wall carbon nanotubes on human HEK293 cells. Toxicol Lett 155(1):73–85. doi:10.1016/j.toxlet.2004.08.015
14. Cveticanin J, Joksic G, Leskovac A, Petrovic S, Sobot AV, Neskovic O (2009) Using carbon nanotubes to induce micronuclei and double strand breaks of the DNA in human cells. Nanotechnology 21(1):015102. doi:10.1088/0957-4484/21/1/015102
15. Davoren M, Herzog E, Casey A et al (2007) In vitro toxicity evaluation of single walled carbon nanotubes on human A549 lung cells. Toxicol In Vitro 21(3):438–448. doi:10.1016/j.tiv.2006.10.007
16. De Jong WH, Borm PJ (2008) Drug delivery and nanoparticles: applications and hazards. Int J Nanomed 3(2):133–149
17. Deng X, Jiab G, Wang H et al (2007) Translocation and fate of multi-walled carbon nanotubes in vivo. Carbon 45(7):1419–1424
18. Doherty GJ, McMahon HT (2009) Mechanisms of endocytosis. Annu Rev Biochem 78:857–902. doi:10.1146/annurev.biochem.78.081307.110540
19. Dong L, Joseph KL, Witkowski CM, Craig MM (2008) Cytotoxicity of single-walled carbon nanotubes suspended in various surfactants. Nanotechnology 19(25):255702. doi:10.1088/0957-4484/19/25/255702
20. Dong L, Witkowski CM, Craig MM, Greenwade MM, Joseph KL (2009) Cytotoxicity effects of different surfactant molecules conjugated to carbon nanotubes on human astrocytoma cells. Nanoscale Res Lett 4(12):1517–1523. doi:10.1007/s11671-009-9429-0
21. Donkor A, Su Z, Mandal H, Jin X, Tang X (2009) Carbon nanotubes inhibit the hemolytic activity of the pore-forming toxin pyolysin. Nano Res 2(7):517–525. doi:10.1007/s12274-009-9049-0
22. Dumortier H, Lacotte S, Pastorin G et al (2006) Functionalized carbon nanotubes are non-cytotoxic and preserve the functionality of primary immune cells. Nano Lett 6(7):1522–1528. doi:10.1021/nl061160x
23. Dutta D, Sundaram SK, Teeguarden JG et al (2007) Adsorbed proteins influence the biological activity and molecular targeting of nanomaterials. Toxicol Sci 100(1):303–315. doi:10.1093/toxsci/kfm217
24. El-Ansary A, Al-Daihan S (2009) On the toxicity of therapeutically used nanoparticles: an overview. J Toxicol 2009:754810. doi:10.1155/2009/754810
25. Folkmann JK, Risom L, Jacobsen NR, Wallin H, Loft S, Moller P (2009) Oxidatively damaged DNA in rats exposed by oral gavage to C60 fullerenes and single-walled carbon nanotubes. Environ Health Perspect 117(5):703–708. doi:10.1289/ehp.11922
26. Ge C, Du J, Zhao L et al (2011) Binding of blood proteins to carbon nanotubes reduces cytotoxicity. Proc Natl Acad Sci USA 108(41):16968–16973. doi:10.1073/pnas.1105270108
27. Geiser M, Rothen-Rutishauser B, Kapp N et al (2005) Ultrafine particles cross cellular membranes by nonphagocytic mechanisms in lungs and in cultured cells. Environ Health Perspect 113(11):1555–1560
28. Girifalco L, Hodak M, Lee RS (2000) Carbon nanotubes, buckyballs, ropes, and a universal graphitic potential. Phys Rev B 62(19):13104
29. Gutierrez-Praena D, Pichardo S, Sanchez E, Grilo A, Camean AM, Jos A (2011) Influence of carboxylic acid functionalization on the cytotoxic effects induced by single wall carbon nanotubes on human endothelial cells (HUVEC). Toxicol In Vitro 25(8):1883–1888. doi:10.1016/j.tiv.2011.05.027
30. Hitoshi K, Katoh M, Suzuki T, Ando Y, Nadai M (2012) Changes in expression of drug-metabolizing enzymes by single-walled carbon nanotubes in human respiratory tract cells. Drug Metab Dispos 40(3):579–587. doi:10.1124/dmd.111.043455
31. Huczko A, Lange H (2001) Carbon nanotubes: experimental evidence for a null risk of skin irritation and allergy. Fuller Sci Technol 9(2):247–250
32. Huczko A, Lange H, Całko E, Grubek-Jaworska H, Droszcz P (2001) Physiological testing of carbon nanotubes: are they asbestos-like? Fuller Sci Technol 9(2):251–254
33. Iversen T-G, Skotland T, Sandvig K (2011) Endocytosis and intracellular transport of nanoparticles: present knowledge and need for future studies. Nano Today 6(2):176–185
34. Jia G, Wang H, Yan L et al (2005) Cytotoxicity of carbon nanomaterials: single-wall nanotube, multi-wall nanotube, and fullerene. Environ Sci Technol 39(5):1378–1383
35. Jin H, Heller DA, Strano MS (2008) Single-particle tracking of endocytosis and exocytosis of single-walled carbon nanotubes in NIH-3T3 cells. Nano Lett 8(6):1577–1585. doi:10.1021/nl072969s
36. Johnson DR, Methner MM, Kennedy AJ, Steevens JA (2010) Potential for occupational exposure to engineered carbon-based nanomaterials in environmental laboratory studies. Environ Health Perspect 118(1):49–54. doi:10.1289/ehp.0901076
37. Kagan VE, Tyurina YY, Tyurin VA et al (2006) Direct and indirect effects of single walled carbon nanotubes on RAW 264.7 macrophages: role of iron. Toxicol Lett 165(1):88–100. doi:10.1016/j.toxlet.2006.02.001
38. Kam NW, Liu Z, Dai H (2006) Carbon nanotubes as intracellular transporters for proteins and DNA: an investigation of the uptake mechanism and pathway. Angew Chem Int Ed Engl 45(4):577–581. doi:10.1002/anie.200503389
39. Klumpp C, Kostarelos K, Prato M, Bianco A (2006) Functionalized carbon nanotubes as emerging nanovectors for the delivery of therapeutics. Biochim Biophys Acta 1758(3):404–412. doi:10.1016/j.bbamem.2005.10.008
40. Krajcik R, Jung A, Hirsch A, Neuhuber W, Zolk O (2008) Functionalization of carbon nanotubes enables non-covalent binding and intracellular delivery of small interfering RNA for efficient knock-down of genes. Biochem Biophys Res Commun 369(2):595–602. doi:10.1016/j.bbrc.2008.02.072
41. Lam CW, James JT, McCluskey R, Hunter RL (2004) Pulmonary toxicity of single-wall carbon nanotubes in mice 7 and 90 days after intratracheal instillation. Toxicol Sci 77(1):126–134. doi:10.1093/toxsci/kfg243
42. 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(3):189–217
43. Lee J, Mahendra S, Alvarez PJ (2010) Nanomaterials in the construction industry: a review of their applications and environmental health and safety considerations. ACS Nano 4(7):3580–3590. doi:10.1021/nn100866w
44. Legramante JM, Valentini F, Magrini A et al (2009) Cardiac autonomic regulation after lung exposure to carbon nanotubes. Hum Exp Toxicol 28(6–7):369–375. doi:10.1177/0960327109105150
45. Li JG, Li WX, Xu JY et al (2007a) Comparative study of pathological lesions induced by multiwalled carbon nanotubes in lungs of mice by intratracheal instillation and inhalation. Environ Toxicol 22(4):415–421. doi:10.1002/tox.20270
46. Li Z, Hulderman T, Salmen R et al (2007b) Cardiovascular effects of pulmonary exposure to single-wall carbon nanotubes. Environ Health Perspect 115(3):377–382. doi:10.1289/ehp.9688
47. Liu Z, Cai W, He L et al (2007) In vivo biodistribution and highly efficient tumour targeting of carbon nanotubes in mice. Nat Nanotechnol 2(1):47–52. doi:10.1038/nnano.2006.170
48. Liu Z, Tabakman SM, Chen Z, Dai H (2009) Preparation of carbon nanotube bioconjugates for biomedical applications. Nat Protoc 4(9):1372–1382. doi:10.1038/nprot.2009.146
49. Mahar B, Laslau C, Yip R, Sun Y (2007) Development of carbon nanotube-based sensors—a review. Sens J IEEE 7(2):266–284
50. Mangum JB, Turpin EA, Antao-Menezes A, Cesta MF, Bermudez E, Bonner JC (2006) Single-walled carbon nanotube (SWCNT)-induced interstitial fibrosis in the lungs of rats is associated with increased levels of PDGF mRNA and the formation of unique intercellular carbon structures that bridge alveolar macrophages in situ. Part Fibre Toxicol 3:15. doi:10.1186/1743-8977-3-15
51. Mauter MS, Elimelech M (2008) Environmental applications of carbon-based nanomaterials. Environ Sci Technol 42(16):5843–5859
52. Maynard A, Michelson E (2006) The nanotechnology consumer products inventory. Woodrow Wilson International Center for Scholars, Washington, DC, Accessed March 23
53. Maynard AD, Baron PA, Foley M, Shvedova AA, Kisin ER, Castranova V (2004) Exposure to carbon nanotube material: aerosol release during the handling of unrefined single-walled carbon nanotube material. J Toxicol Environ Health A 67(1):87–107. doi:10.1080/15287390490253688
54. McDevitt MR, Chattopadhyay D, Jaggi JS et al (2007a) PET imaging of soluble yttrium-86-labeled carbon nanotubes in mice. PLoS One 2(9):e907. doi:10.1371/journal.pone.0000907
55. McDevitt MR, Chattopadhyay D, Kappel BJ et al (2007b) Tumor targeting with antibody-functionalized, radiolabeled carbon nanotubes. J Nucl Med 48(7):1180–1189. doi:10.2967/jnumed.106.039131
56. Monteiro-Riviere NA, Inman AO (2006) Challenges for assessing carbon nanomaterial toxicity to the skin. Carbon 44(6):1070–1078
57. 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(2):222–235. doi:10.1016/j.taap.2008.09.030
58. Murr LE (2008) Microstructures and nanostructures for environmental carbon nanotubes and nanoparticulate soots. Int J Environ Res Public Health 5(5):321–336
59. Murr LE, Bang JJ, Esquivel EV, Guerrero PA, Lopez DA (2004) Carbon nanotubes and nanocrystal forms, and complex nanoparticle aggregates in common fuel-gas combustion sources and the ambient air. J Nanopart Res 6:241–251
60. Murr LE, Garza KM, Soto KF et al (2005) Cytotoxicity assessment of some carbon nanotubes and related carbon nanoparticle aggregates and the implications for anthropogenic carbon nanotube aggregates in the environment. Int J Environ Res Public Health 2(1):31–42
61. Murray AR, Kisin E, Leonard SS et al (2009) Oxidative stress and inflammatory response in dermal toxicity of single-walled carbon nanotubes. Toxicology 257(3):161–171. doi:10.1016/j.tox.2008.12.023
62. Oh N, Park JH (2014) Endocytosis and exocytosis of nanoparticles in mammalian cells. Int J Nanomed 9(Suppl 1):51–63. doi:10.2147/IJN.S26592
63. Pacurari M, Yin XJ, Zhao J et al (2008) 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 116(9):1211–1217. doi:10.1289/ehp.10924
64. Pantarotto D, Partidos CD, Hoebeke J et al (2003) Immunization with peptide-functionalized carbon nanotubes enhances virus-specific neutralizing antibody responses. Chem Biol 10(10):961–966
65. Park EJ, Roh J, Kim SN, et al (2011) A single intratracheal instillation of single-walled carbon nanotubes induced early lung fibrosis and subchronic tissue damage in mice. Arch Toxicol 85(9):1121–1131. doi:10.1007/s00204-011-0655-8
66. Pichardo S, Gutierrez-Praena D, Puerto M et al (2012) Oxidative stress responses to carboxylic acid functionalized single wall carbon nanotubes on the human intestinal cell line Caco-2. Toxicol In Vitro 26(5):672–677. doi:10.1016/j.tiv.2012.03.007
67. Poland CA, Duffin R, Kinloch I et al (2008) Carbon nanotubes introduced into the abdominal cavity of mice show asbestos-like pathogenicity in a pilot study. Nat Nanotechnol 3(7):423–428. doi:10.1038/nnano.2008.111
68. Porter AE, Gass M, Muller K, Skepper JN, Midgley PA, Welland M (2007) Direct imaging of single-walled carbon nanotubes in cells. Nat Nanotechnol 2(11):713–717. doi:10.1038/nnano.2007.347
69. Rothen-Rutishauser BM, Schurch S, Haenni B, Kapp N, Gehr P (2006) Interaction of fine particles and nanoparticles with red blood cells visualized with advanced microscopic techniques. Environ Sci Technol 40(14):4353–4359
70. Sachar S, Saxena RK (2011) Cytotoxic effect of poly-dispersed single walled carbon nanotubes on erythrocytes in vitro and in vivo. PLoS One 6(7):e22032. doi:10.1371/journal.pone.0022032
71. Sahaym U, Norton MG (2008) Advances in the application of nanotechnology in enabling a ‘hydrogen economy’. J Mater Sci 43(16):5395–5429
72. Sayes CM, Liang F, Hudson JL et al (2006) Functionalization density dependence of single-walled carbon nanotubes cytotoxicity in vitro. Toxicol Lett 161(2):135–142. doi:10.1016/j.toxlet.2005.08.011
73. Schipper ML, Nakayama-Ratchford N, Davis CR et al (2008) A pilot toxicology study of single-walled carbon nanotubes in a small sample of mice. Nat Nanotechnol 3(4):216–221. doi:10.1038/nnano.2008.68
74. Shang L, Nienhaus K, Nienhaus GU (2014) Engineered nanoparticles interacting with cells: size matters. J Nanobiotechnol 12:5. doi:10.1186/1477-3155-12-5
75. Shvedova AA, Kisin ER, Mercer R et al (2005) Unusual inflammatory and fibrogenic pulmonary responses to single-walled carbon nanotubes in mice. Am J Physiol Lung Cell Mol Physiol 289(5):L698–L708. doi:10.1152/ajplung.00084.2005
76. Shvedova AA, Kisin ER, Murray AR et al (2007) Vitamin E deficiency enhances pulmonary inflammatory response and oxidative stress induced by single-walled carbon nanotubes in C57BL/6 mice. Toxicol Appl Pharmacol 221(3):339–348. doi:10.1016/j.taap.2007.03.018
77. Shvedova AA, Kisin E, Murray AR et al (2008) 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 295(4):L552–L565. doi:10.1152/ajplung.90287.2008
78. Singh R, Pantarotto D, Lacerda L et al (2006) Tissue biodistribution and blood clearance rates of intravenously administered carbon nanotube radiotracers. Proc Natl Acad Sci USA 103(9):3357–3362. doi:10.1073/pnas.0509009103
79. Sun L, Zhang Y (2008) The biocompatibility of carbon nanotubes. Sheng Wu Yi Xue Gong Cheng Xue Za Zhi 25(3):742–746
80. Tang T, Chen X, Meng X, Chen H, Ding Y (2005) Synthesis of multiwalled carbon nanotubes by catalytic combustion of polypropylene. Angew Chem Int Ed Engl 44(10):1517–1520. doi:10.1002/anie.200461506
81. Tong L, Liu Y, Dolash BD et al (2012) Label-free imaging of semiconducting and metallic carbon nanotubes in cells and mice using transient absorption microscopy. Nat Nanotechnol 7(1):56–61. doi:10.1038/nnano.2011.210
82. Tyurina YY, Kisin ER, Murray A et al (2011) Global phospholipidomics analysis reveals selective pulmonary peroxidation profiles upon inhalation of single-walled carbon nanotubes. ACS Nano 5(9):7342–7353. doi:10.1021/nn202201j
83. Villa CH, McDevitt MR, Escorcia FE et al (2008) Synthesis and biodistribution of oligonucleotide-functionalized, tumor-targetable carbon nanotubes. Nano Lett 8(12):4221–4228. doi:10.1021/nl801878d
84. Warheit DB, Laurence BR, Reed KL, Roach DH, Reynolds GA, Webb TR (2004) Comparative pulmonary toxicity assessment of single-wall carbon nanotubes in rats. Toxicol Sci 77(1):117–125. doi:10.1093/toxsci/kfg228
85. Worle-Knirsch JM, Pulskamp K, Krug HF (2006) Oops they did it again! Carbon nanotubes hoax scientists in viability assays. Nano Lett 6(6):1261–1268. doi:10.1021/nl060177c
86. Wu M, Gordon RE, Herbert R et al (2010) Case report: lung disease in World Trade Center responders exposed to dust and smoke: carbon nanotubes found in the lungs of World Trade Center patients and dust samples. Environ Health Perspect 118(4):499–504. doi:10.1289/ehp.0901159
87. Yang J, Li W, Li Q, Wu S, Yu B, Jing X (2007a) Oxygen adsorption by carbon nanotubes and its application in radiotherapy. IET Nanobiotechnol 1(1):10–14. doi:10.1049/iet-nbt:20060017
88. Yang S-T, Guo W, Lin Y et al (2007b) Biodistribution of pristine single-walled carbon nanotubes in vivo. J Phys Chem C 111(48):17761–17764
89. Yang Z, Zhang Y, Yang Y et al (2010) Pharmacological and toxicological target organelles and safe use of single-walled carbon nanotubes as drug carriers in treating Alzheimer disease. Nanomedicine 6(3):427–441. doi:10.1016/j.nano.2009.11.007
90. Zhang S, Li J, Lykotrafitis G, Bao G, Suresh S (2009) Size-Dependent Endocytosis of Nanoparticles. Adv Mater 21:419–424. doi:10.1002/adma.200801393
91. Zhang Y, Bai Y, Yan B (2010) Functionalized carbon nanotubes for potential medicinal applications. Drug Discov Today 15(11–12):428–435. doi:10.1016/j.drudis.2010.04.005
92. Zhao Y, Xing G, Chai Z (2008) Nanotoxicology: are carbon nanotubes safe? Nat Nanotechnol 3(4):191–192. doi:10.1038/nnano.2008.77