Imaging methods for determining uptake and toxicity of carbon nanotubes in vitro and in vivo

Nanomedicine

Volumn 6, Issue 5, 2011, Pages 849-865

  Nerl, Hannah C ^a   Cheng, Crystal ^b   Goode, Angela E ^a   Bergin, Shane D ^c   Lich, Ben ^d   Gass, Mhairi ^e   Porter, Alexandra E ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c Imperial College London South Kensington Campus ^*  (United Kingdom)

^d Thermo Fisher Scientific   (United States)

^e DARESBURY LABORATORY   (United Kingdom)

Author keywords

carbon nanotubes; cell uptake; electron microscopy; toxicity assays

Indexed keywords

MULTI WALLED NANOTUBE; REACTIVE OXYGEN METABOLITE; SINGLE WALLED NANOTUBE;

CELL STRUCTURE; CELL VIABILITY; CULTURE MEDIUM; DISPERSION; ELECTRON ENERGY LOSS SPECTROSCOPY; HUMAN; NONHUMAN; PARTICLE SIZE; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; REVIEW; SCANNING ELECTRON MICROSCOPY; TOXICITY; TRANSMISSION ELECTRON MICROSCOPY;

ANIMALS; CELL MEMBRANE PERMEABILITY; HUMANS; MICROSCOPY; NANOTUBES, CARBON; TOXICITY TESTS;

EID: 79960953783     PISSN: 17435889     EISSN: 17486963     Source Type: Journal    
DOI: 10.2217/nnm.11.87     Document Type: Review

References (65)

1. Kroto HW, Heath JR, O'Brien SC, Curl RF, Smalley RE. C60: buckminsterfullerene. Nature 318, 162-163 (1985).
2. Meyyappan M. Carbon nanotube Scienceand technology. CRC 1-304 (2005).
3. Poland CAR, Duffin I, Kinloch A et al. Carbon nanotubes introduced into the abdominal cavity of mice show asbestos-like pathogenicity in a pilot study. Nat. Nanotechnol. 3, 423-428 (2008).
4. Porter DW, Hubbs AF, Mercer RR et al. Mouse pulmonary dose-and time course-responses induced by exposure to multi-walled carbon nanotubes. Toxicology 269(2-3), 136-147 (2009).
5. Li JG, Li WX, Xu JY et al. Comparative study of pathological lesions induced by multiwalled carbon nanotubes in lungs of mice by intratracheal instillation and inhalation. Environ. Toxicol. 22, 415-421 (2007).
6. Yamashita K, Yoshioka Y, Higashisaka K et al. Carbon nanotubes elicit DNA damage and inflammatory response relative to their size and shape. Inflammation 33(4), 276-280 (2010).
7. Ryman-Rasmussen JP, Cesta MF, Brody AR et al. Inhaled carbon nanotubes reach the subpleural tissue in mice. Nat. Nanotechnol. 4(11), 747-751 (2009).
8. Lacerda L, Soundararajan A, Singh R et al. Dynamic imaging of functionalized multi-walled carbon nanotube systemic circulation and urinary excretion. Adv. Mater. 20(2), 225-230 (2008). (Pubitemid 351205693)
9. Bottini M, Bruckner S, Nika K et al. Multi-walled carbon nanotubes induce T lymphocyte apoptosis. Toxicol. Lett. 160(2), 121-126 (2006). (Pubitemid 41578955)
10. Hirano S, Kanno S, Furuyama A. Multi-walled carbon nanotubes injure the plasma membrane of macrophages. Toxicol. Appl. Pharmacol. 232(2), 244-251 (2008).
11. Simon-Deckers A, Gouget B, Mayne-L'hermite M, Herlin-Boime N, Reynaud C, Carrière M. In vitro investigation of oxide nanoparticle and carbon nanotube toxicity and intracellular accumulation in A549 human pneumocytes. Toxicology 253(1-3), 137-146 (2008).
12. Ding L, Stilwell J, Zhang T et al. Molecular characterization of the cytotoxic mechanism of multiwall carbon nnaotubes and non-onions on human skin fibroblast. Nano Lett. 5(120), 2448-2464 (2005). (Pubitemid 43090840)
13. Johnston HJ, Hutchison GR, Christensen FM et al. A critical review of the biological mechanisms underlying the in vivo and in vitro toxicity of carbon nanotubes: the contribution of physico-chemical characteristics. Nanotoxicology 4, 207-246 (2010).
14. Pacurari M, Castranova V, Vallyathan V. Single-and multi-wall carbon nanotubes versus asbestos: are the carbon nanotubes a new health risk to humans? J. Toxicol. Environ. Health A. 73(5), 378-395 (2010).
15. Kateb B, Van Handel M, Zhang L, Bronikowski MH, Manohara H, Badie B. Internernalization of MWNTs by microglia: possible application in immunotherapy of brain tumours. Neuroimage 37(Suppl. 1), S9-S17 (2007). (Pubitemid 47239427)
16. Pulskamp K, Diabete S, Krug HF. Carbon nanotubes show no sign of acute toxicity but induce intracellular reactive oxygen species in dependence on contaminants. Toxicol. Lett. 168(1), 58-74 (2007). (Pubitemid 44909723)
17. Grabinski C, Hussain S, Lafdi K, Braydich-Stolle L, Schlager J. Effect of particle dimension on biocompatibility of carbon nanomaterials. Carbon 45(14), 2828-2835 (2007). (Pubitemid 350086566)
18. Schrand AM, Dai L, Schlager JJ, Hussain SM, Osawa E. Differential bio compatibly of carbon nanotubes and nanodiamonds. Diamond Relat. Mater. 16(12), 2118-2123 (2007). (Pubitemid 350117432)
19. Shvedova AA, Castranova V, Kisin ER et al. Exposure to carbon nanotube material: assessment of nanotube cytotoxicity using human keratinocyte cells. J. Toxicol. Environ. Health A 66(20), 1909-1926 (2003). (Pubitemid 37352634)
20. Sayes CM, Liang F, Hudson JL et al. Functionalization density dependence of single-walled carbon nanotubes cytotoxicity in vitro. Toxicol. Lett. 161(2), 135-142 (2006). (Pubitemid 41790286)
21. Menzel R, Lee A, Bismarck A et al. Inverse gas chromatography of as-received and modified carbon nanotubes. Langmuir 25, 8340-8348 (2009).
22. Kostarelos K, Lacerda L, Pastorin G et al. Cellular uptake of functionalized carbon nanotubes is independent of functional group and cell type. Nat. Nanotech. 2, 108-113 (2007). (Pubitemid 46230832)
23. Mu Q, Broughton DL, Yan B. Endosomal leakage and nuclear translocation of multiwalled carbon nanotubes: developing a model for cell uptake. Nano Lett. 9(12), 4370-4375 (2009).
24. Brown DM, Kinloch IA, Bangert U et al. An in vitro study of the potential of carbon nanotubes and nanofibres to induce inflammation mediators and frustrated phagocytosis. Carbon 45, 1743-1756 (2007). (Pubitemid 47069251)
25. Lam CW, James JT, McCluskey R, Hunter RL. Pulmonary toxicity of single-wall carbon nanotubes in mice 7 and 90 days after intratracheal instillation. Toxicol. Sci. 77, 126-134 (2004). (Pubitemid 38128652)
26. Elgrabli D, Abella-Gallart S, Robidel F, Rogerieux F, Boczkowski J, Lacroix G. Induction of apoptosis and absence of inflammation in rat lung after intratracheal instillation of multiwalled carbon nanotubes. Toxicology 253, 131-136 (2008).
27. De Nicola M, Bellucci S, Traversa E, De Bellis G, Micciulla F, Ghibelli L. Carbon nanotubes on Jurkat cells: effects on cell viability and plasma membrane potential. J. Phys. Condens. Matt. 20(47), 474204 (2008).
28. Jia G, Wang H, Wang LYX et al. Cytoxicity of carbon nanomaterials: single-wall nanotube, multi-wall nanotube and fullerene. Environ. Sci. Technol. 39(5), 1378-1383 (2005). (Pubitemid 40333400)
29. Zhang D, Yi C, Zhang J, Chen Y, Yao X, Yang M. The effects of carbon nanotubes on the proliferation and differentiation of primary osteoblasts. Nanotechnology 18(47), 475102 (2007).
30. Davoren M, Herzog E, Casey A et al. In vitro toxicity evaluation of single walled carbon nanotubes on human A549 lung cells. Toxicol. In Vitro 21(2), 438-448 (2007). (Pubitemid 46453117)
31. Jacobsen NR, Opjana G, White P et al. Genotoxicity, cytotoxicity and reactive oxygen species induced by single-walled carbon nanotubes and C60 fullerenes in the FE1-Muta mouse lung epithalial cells. Environ. Mol. Mutagen. 49(6), 476-487 (2008).
32. Zeni O, Palumbo R, Bernini R, Zeni L, Sarti M, Scarfi MR. Cytotoxicity investigation on cultured human blood cells treated with single-wall carbon nanotubes. Sensors 8(1), 488-499 (2008).
33. Herzog E, Byrne HJ, Casey A et al. SWCNT suppress inflammatory mediator responses in human lung epithelium in vitro. Toxicol. Appl. Pharmacol. 234(3), 378-390 (2009).
34. Cui HF, Vashist SK, Al-Rubeaan K, Luong JH, Sheu FS. Interfacing carbon nanotubes with living mammalian cells and cytotoxicity issues. Chem. Res. Toxicol. 23(7), 1131-1147 (2010).
35. Pacurari M, Yun XJ, Zhao J et al. Raw single-wall carbon nanotubes induce oxidative stress and activate MAPKs, AP-1, NF-kB and Akt in normal and malignant human mesothelial cells. Environ. Health Perspect. 116(9), 1211-1217 (2008).
36. Shvedova A, Kisin E, Murray A et al. Exposure of human bronchial cells to carbon nanotubes caused oxidative stress and cytotoxicity. Proceedings of the meeting of the SFRR Europe. 26-29 June 2003, 88-7587-002; 88-7587-003-9 (2004).
37. Wick P, Manser P, Limback LK et al. The degree and kind of agglomeration affect carbon nanotube cytotoxicity. Toxicol. Lett. 168(2), 121-131 (2007). (Pubitemid 46054362)
38. Porter AE, Gass M, Bendall JS et al. Uptake of noncytotoxic acid-treated single-walled carbon nanotubes into the cytoplasm of human macrophage cells. ACS Nano 3(6), 1485-1492 (2009).
39. Alpatova AL, Shan W, Babica P et al. Single-walled carbon nanotubes dispersed in aqueous media via non-covalent functionalization: effect of dispersant on the stability, cytotoxicity, and epigenetic toxicity of nanotube suspensions. Water Res. 44(2), 505-520 (2009).
40. Monteiro-Riviere NA, Inman AO, Zhang LW. Limitations and relative utility of screening assays to assess engineered nanoparticle toxicity in a human cell line. Toxiol. Appl. Pharmacol. 234(2), 222-235 (2009).
41. Shvedova AA, Kisin ER, Mercer R et al. Unusual inflammatory and fibrogenic pulmonary responses to single walled carbon nanotubes in mice. Am. J. Physiol. Lung Cell. Mol. Physiol. 289, 698-708 (2005).
42. Ravichandran P, Periyakaruppan A, Sadanandan B et al. Induction of apoptosis in rat lung epithelial cells by multiwalled carbon nanotubes. J. Biochem. Mol. Toxicol. 23(5) 333-334 (2009).
43. Motskin M, Wright DM, Muller K et al. Hydroxyapatite nano and microparticles: correlation of particle properties with cytotoxicity and biostability. Biomaterials 30(19), 3307-3317 (2009).
44. Muller KH, Kulkarni J, Motskin M et al. pH-dependent toxicity of high aspect ratio ZnO nanowires in macrophages due to intracellular dissolution. ACS Nano 4(11), 6767-6779 (2010).
45. Mu Q, Broughton DL, Yan B. Endosomal leakage and nuclear translocation of multiwalled carbon nanotubes: developing a model for cell uptake. Nano Lett. 9(12), 4370-4375 (2009).
46. Raffa V, Ciofani G, Vittorio O, Riggio C, Cuschieri A. Physicochemical properties affecting cellular uptake of carbon nanotubes. Nanomedicine (Lond.) 5(1), 89-97 (2010).
47. Jin H, Heller DA, Strano MS. Single-particle tracking of endocytosis and exocytosis of single-walled carbon nanotubes in NIH-3T3 cells. Nano Lett. 8(6), 1577-1585 (2008).
48. Allen BL, Kichambare PD, Gou P et al. Biodegradation of single-walled carbon nanotubes through enzymatic catalysis. Nano Lett. 8(11), 3899-3903 (2008).
49. Kagan VE, Konduru NV, Feng W et al. Carbon nanotubes degraded by neutrophil myeloperoxidase induce less pulmonary inflammation. Nat. Nanotechnol. 5(5), 354-359 (2010).
50. Cheng C, Muller K, Koziol K et al. Toxicity and imaging of multi-walled carbon nanotubes in human macrophage cells. Biomaterials 30(25), 4152-4160 (2009).
51. Porter AE, Gass M, Muller K, Skepper JN, Midgley PA, Welland M. Direct imaging of single-walled carbon nanotubes in cells. Nat. Nanotechnol. 2(11), 713-717 (2007). (Pubitemid 350071068)
52. Hardwick SJ, Hegyi L, Clare K et al. Apoptosis in human monocyte-macrophages exposed to oxidized low density lipoprotein. J. Pathol. 179, 294-302 (1996). (Pubitemid 26266409)
53. Sloan J, Kirkland AI, Hutchinson JL, Green MLH. Aspects of crystal growth within carbon nanotubes. CR Phys. 4, 1063-1074 (2003). (Pubitemid 38012002)
54. Porter AE, Gass M, Muller K, Skepper J, Midgley P, Welland M. Visualizing the uptake of C60 to the cytoplasm and nucleus of human monocyte-derived macrophage cells using energy-filtered transmission electron microscopy and electron tomography. Environ. Sci. Technol. 41(8), 3012-3017 (2007). (Pubitemid 46626435)
55. Stockli T, Bonard JM, Chatelain A. Plasmon excitations in graphitic carbon spheres measured by EELS. Phys. Rev. B 61, 5751-5759 (2000).
56. Suenaga K, Koshino M. Atom-by-atom spectroscopy at the graphene edge. Nature 468(7327), 1088-1090 (2010).
57. Najafi E, Wang J, Hitchcock AP, Guan J, Denomme S, Simard B. Characterization of single-walled carbon nanotubes by scanning transmission x-ray spectromicroscopy: purification, order and dodecyl functionalization. J. Am. Chem. Soc. 132(26), 9020-9029 (2010).
58. Midgley PA, Weyland M. 3D electron microscopy in the physical sciences: the development of Z-contrast and EFTEM tomography. Ultramicroscopy 96, 413 (2003).
59. Hohmann-Marriott MF, Sousa AA, Azari AA et al. Nanoscale 3D cellular imaging by axial scanning transmission electron tomography. Nat. Methods 6(10), 729-731 (2009).
60. Knott G, Marchman H, Wall D, Lich B. Serial section scanning electron microscopy of adult brain tissue using focussed ion beam milling. J. Neurosci. 28(12), 2959-2964 (2008). (Pubitemid 351442268)
61. Cui D, Tian F, Ozkan CS, Wang M, Gao H. Effects of single wall carbon nanotubes on human HEK293 cells. Toxicol. Lett. 155(1), 73-85 (2005). (Pubitemid 39600739)
62. Pulskamp K, Diabete S, Drug HF. Carbon nanotubes show no sign of acute toxicity but induce intracellular reactive oxygen species in dependence on contaminants. Toxicol. Lett. 168(1), 58-74 (2007). (Pubitemid 44909723)
63. Singh R, Pantarotto D, Lacerda L et al. Tissue biodistribution and blood clearance rates of intravenously administered carbon nanotube radiotracers. Proc. Natl Acad. Sci. USA 103(9), 3357-3362 (2006). (Pubitemid 43346474)
64. Casey A, Herzog E, Davoren M, Lyng FM, Byrne HJ, Chambers G. Spectroscopic analysis confirms the interactions between single walled carbon nanotubes and various dyes commonly used to assess cytotoxicity. Carbon 45(7), 1425-1432 (2007). (Pubitemid 46829030)
65. Guo L, Von Dem Bussche A, Buechner M, Yan A, Kane AB, Hurt RH. Adsorption of essential micronutrients by carbon nanotubes and the implications for nanotoxicity testing. Small 4(6), 721-727 (2008). (Pubitemid 352007131)