High resolution and dynamic imaging of biopersistence and bioreactivity of extra and intracellular MWNTs exposed to microglial cells

Biomaterials

Volumn 70, Issue , 2015, Pages 57-70

  Goode, Angela E ^a   Gonzalez Carter, Daniel A ^a   Motskin, Michael ^a   Pienaar, Ilse S ^a   Chen, Shu ^a   Hu, Sheng ^a   Ruenraroengsak, Pakatip ^a   Ryan, Mary P ^a   Shaffer, Milo S P ^a   Dexter, David T ^a   Porter, Alexandra E ^a  

^a IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

Aggregation; Biocompatibility; Brain; Carbon nanotube (CNT); Microglia

Indexed keywords

AGGLOMERATION; AGGREGATES; BIOCOMPATIBILITY; BIODEGRADATION; BRAIN; CARBON; CARBON NANOTUBES; CYTOLOGY; ELECTRON MICROSCOPY; ENZYME ACTIVITY; HIGH RESOLUTION TRANSMISSION ELECTRON MICROSCOPY; ION BEAMS; MULTIWALLED CARBON NANOTUBES (MWCN); NITRIC OXIDE; SCAFFOLDS (BIOLOGY); SCANNING ELECTRON MICROSCOPY; TISSUE REGENERATION; TRANSMISSION ELECTRON MICROSCOPY; ULTRAVIOLET VISIBLE SPECTROSCOPY; YARN;

CORRELATIVE APPROACHES; EXTRACELLULAR ENVIRONMENTS; GRAPHITIC STRUCTURES; MICROGLIA; MULTISCALE TECHNIQUE; REACTIVE OXYGEN SPECIES; THERAPEUTIC DRUG DELIVERY; UV-VIS SPECTROSCOPY;

OXIDATION;

INTERLEUKIN 1BETA; INTERLEUKIN 6; MULTI WALLED NANOTUBE; NITRIC OXIDE; REACTIVE OXYGEN METABOLITE; TUMOR NECROSIS FACTOR ALPHA; CARBON NANOTUBE; CYTOKINE;

ANIMAL CELL; ARTICLE; BIODEGRADATION; CELL VIABILITY; CONTROLLED STUDY; CYTOKINE RELEASE; CYTOPLASM; INTERNALIZATION; MICROGLIA; MOUSE; NONHUMAN; OXIDATION; PHAGOCYTOSIS; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; SCANNING ELECTRON MICROSCOPY; TRANSMISSION ELECTRON MICROSCOPY; ULTRAVIOLET SPECTROSCOPY; ANIMAL; BIOSYNTHESIS; CELL SURVIVAL; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; ENDOCYTOSIS; EXTRACELLULAR SPACE; INTRACELLULAR SPACE; OXIDATION REDUCTION REACTION; PROCEDURES; THREE DIMENSIONAL IMAGING; ULTRASTRUCTURE; ULTRAVIOLET SPECTROPHOTOMETRY;

ANIMALS; CELL SURVIVAL; CYTOKINES; ENDOCYTOSIS; EXTRACELLULAR SPACE; IMAGING, THREE-DIMENSIONAL; INTRACELLULAR SPACE; MICE; MICROGLIA; NANOTUBES, CARBON; OXIDATION-REDUCTION; SPECTROPHOTOMETRY, ULTRAVIOLET;

EID: 84940845216     PISSN: 01429612     EISSN: 18785905     Source Type: Journal    
DOI: 10.1016/j.biomaterials.2015.08.019     Document Type: Article

References (62)

1. Bhirde A.A., Patel V., Gavard J., Zhang G.F., Sousa A.A., Masedunskas A., et al. Targeted killing of cancer cells in vivo and in vitro with EGF-directed carbon nanotube-based drug delivery. ACS Nano 2009, 3:307-316.
2. Kam N.W.S., O'Connell M., Wisdom J.A., Dai H.J. Carbon nanotubes as multifunctional biological transporters and near-infrared agents for selective cancer cell destruction. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:11600-11605.
3. Klumpp C., Kostarelos K., Prato M., Bianco A. Functionalized carbon nanotubes as emerging nanovectors for the delivery of therapeutics. BBA Biomembranes 2006, 1758:404-412.
4. Bussy C., Al-Jamal K.T., Boczkowski J., Lanone S., Prato M., Bianco A., et al. Microglia determine brain region-specific neurotoxic responses to chemically functionalized carbon nanotubes. ACS Nano 2015, 10.1021/acsnano.5b02358.
5. Kafa H., Wang J.T.W., Rubio N., Venner K., Anderson G., Pach E., et al. The interaction of carbon nanotubes with an in vitro blood-brain barrier model and mouse brain in vivo. Biomaterials 2015, 53:437-452.
6. Wang N., Feng Y., Zeng L., Zhao Z., Chen T. Functionalized multiwalled carbon nanotubes as carriers of ruthenium complexes to antagonize cancer multidrug resistance and radioresistance. ACS Appl. Mater. Interfaces 2015, 7:14933-14945.
7. Yang S.T., Guo W., Lin Y., Deng X.Y., Wang H.F., Sun H.F., et al. Biodistribution of pristine single-walled carbon nanotubes in vivo. J. Phys. Chem. C 2007, 111:17761-17764.
8. Ren J.F., Shen S., Wang D.G., Xi Z.J., Guo L.R., Pang Z.Q., et al. The targeted delivery of anticancer drugs to brain glioma by PEGylated oxidized multi-walled carbon nanotubes modified with angiopep-2. Biomaterials 2012, 33:3324-3333.
9. Lee H.J., Park J., Yoon O.J., Kim H.W., Lee D.Y., Kim D.H., et al. Amine-modified single-walled carbon nanotubes protect neurons from injury in a rat stroke model. Nat. Nanotechnol. 2011, 6:120-124.
10. Voge C.M., Stegemann J.P. Carbon nanotubes in neural interfacing applications. J. Neural Eng. 2011, 8.
11. Al-Jamal K.T., Gherardini L., Bardi G., Nunes A., Guo C., Bussy C., et al. Functional motor recovery from brain ischemic insult by carbon nanotube-mediated siRNA silencing. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:10952-10957.
12. Gällentoft L., Pettersson L.M.E., Danielsen N., Schouenborg J., Prinz C.N., Linsmeier C.E. Size-dependent long-term tissue response to biostable nanowires in the brain. Biomaterials 2015, 42:172-183.
13. Bardi G., Tognini P., Ciofani G., Raffa V., Costa M., Pizzorusso T. Pluronic-coated carbon nanotubes do not induce degeneration of cortical neurons in vivo and in vitro. Nanomed. Nanotechnol. 2009, 5:96-104.
14. Kateb B., Van Handel M., Zhang L., Bronikowski M.J., Manohara H., Badie B. Internalization of MWCNTs by microglia: possible application in immunotherapy of brain tumors. Neuroimage 2007, 37(Suppl. 1):S9-S17.
15. Sato Y., Yokoyama A., Shibata K., Akimoto Y., Ogino S., Nodasaka Y., et al. Influence of length on cytotoxicity of multi-walled carbon nanotubes against human acute monocytic leukemia cell line THP-I in vitro and subcutaneous tissue of rats in vivo. Mol. Biosyst. 2005, 1:176-182.
16. Sayes C.M., Liang F., Hudson J.L., Mendez J., Guo W.H., Beach J.M., et al. Functionalization density dependence of single-walled carbon nanotubes cytotoxicity in vitro. Toxicol. Lett. 2006, 161:135-142.
17. Wick P., Manser P., Limbach L.K., Dettlaff-Weglikowska U., Krumeich F., Roth S., et al. The degree and kind of agglomeration affect carbon nanotube cytotoxicity. Toxicol. Lett. 2007, 168:121-131.
18. Poland C.A., Duffin R., Kinloch I., Maynard A., Wallace W.A.H., Seaton A., et al. Carbon nanotubes introduced into the abdominal cavity of mice show asbestos-like pathogenicity in a pilot study. Nat. Nanotechnol. 2008, 3:423-428.
19. Wang X., Xia T., Ntim S.A., Ji Z.X., Lin S.J., Meng H., et al. Dispersal state of multiwalled carbon nanotubes elicits profibrogenic cellular responses that correlate with fibrogenesis biomarkers and fibrosis in the murine lung. ACS Nano 2011, 5:9772-9787.
20. Al-Jamal K.T., Nunes A., Methven L., Ali-Boucetta H., Li S.P., Toma F.M., et al. Degree of chemical functionalization of carbon nanotubes determines tissue distribution and excretion profile. Angew. Chem. Int. Ed. 2012, 51:6389-6393.
21. Nunes A., Bussy C., Gherardini L., Meneghetti M., Herrero M.A., Bianco A., et al. In vivo degradation of functionalized carbon nanotubes after stereotactic administration in the brain cortex. Nanomedicine 2012, 7:1485-1494.
22. Sato Y., Yokoyama A., Nodasaka Y., Kohgo T., Motomiya K., Matsumoto H., et al. Long-term biopersistence of tangled oxidized carbon nanotubes inside and outside macrophages in rat subcutaneous tissue. Sci. Rep. UK 2013, 3.
23. Jin H., Heller D.A., Strano M.S. Single-particle tracking of endocytosis and exocytosis of single-walled carbon nanotubes in NIH-3T3 cells. Nano Lett. 2008, 8:1577-1585.
24. Bertulli C., Beeson H.J., Hasan T., Huang Y.Y.S. Spectroscopic characterization of protein-wrapped single-wall carbon nanotubes and quantification of their cellular uptake in multiple cell generations. Nanotechnology 2013, 24:14.
25. Holt B.D., Dahl K.N., Islam M.F. Cells take up and recover from protein-stabilized single-wall carbon nanotubes with two distinct rates. ACS Nano 2012, 6:3481-3490.
26. Kettenmann H., Hanisch U.K., Noda M., Verkhratsky A. Physiology of microglia. Physiol. Rev. 2011, 91:461-553.
27. Verdejo R., Lamoriniere S., Cottam B., Bismarck A., Shaffer M. Removal of oxidation debris from multi-walled carbon nanotubes. Chem. Commun. 2007, 513-515.
28. Menzel R., Lee A., Bismarck A., Shaffer M.S.P. Inverse gas chromatography of as-received and modified carbon nanotubes. Langmuir 2009, 25:8340-8348.
29. Chen S., Hu S., Smith E.F., Ruenraroengsak P., Thorley A.J., Menzel R., et al. Aqueous cationic, anionic and non-ionic multi-walled carbon nanotubes, functionalised with minimal framework damage, for biomedical application. Biomaterials 2014, 35:4729-4738.
30. Ruenraroengsak P., Novak P., Berhanu D., Thorley A.J., Valsami-Jones E., Gorelik J., et al. Respiratory epithelial cytotoxicity and membrane damage (holes) caused by amine-modified nanoparticles. Nanotoxicology 2012, 6:94-108.
31. Miranda K.M., Espey M.G., Wink D.A. A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide Biol. Chem. 2001, 5:62-71.
32. Tran M.Q., Tridech C., Alfrey A., Bismarck A., Shaffer M.S.P. Thermal oxidative cutting of multi-walled carbon nanotubes. Carbon 2007, 45:2341-2350.
33. Chen S., Hu S., Smith E.F., Ruenraroengsak P., Thorley A.J., Menzel R., et al. Aqueous cationic, anionic and non-ionic multi-walled carbon nanotubes, functionalised with minimal framework damage, for biomedical application. Biomaterials 2014, 35:4729-4738.
34. Muller K.H., Motskin M., Philpott A.J., Routh A.F., Shanahan C.M., Duer M.J., et al. The effect of particle agglomeration on the formation of a surface-connected compartment induced by hydroxyapatite nanoparticles in human monocyte-derived macrophages. Biomaterials 2014, 35:1074-1088.
35. Righi M., Mori L., Delibero G., Sironi M., Biondi A., Mantovani A., et al. Monokine production by microglial cell clones. Eur. J. Immunol. 1989, 19:1443-1448.
36. Stansley B., Post J., Hensley K. A comparative review of cell culture systems for the study of microglial biology in Alzheimer's disease. J. Neuroinflammation 2012, 9:115.
37. Li Y.Y., Zhang T., Jiang Y.Q., Lee H.F., Schwartz S.J., Sun D.X. (-)-Epigallocatechin-3-gallate inhibits Hsp90 function by impairing Hsp90 association with cochaperones in pancreatic cancer cell line Mia Paca-2. Mol. Pharm. 2009, 6:1152-1159.
38. Miranda K.M., Espey M.G., Wink D.A. A rapid, simple spectrophotometric method for simultaneous detection of nitrate and nitrite. Nitric Oxide 2001, 5:62-71.
39. Kushida T., Iijima H., Kushida H., Tsuruta C. En-bloc staining available for stereoscopic observation of epoxy-resin Quetol-651-embedded thick sections under a high-voltage transmission electron-microscope. J. Electron Microsc. 1991, 40:76-77.
40. Luzzi D.E., Smith B.W. Electron irradiation effects in single wall carbon nanotubes. J. Appl. Phys. 2001, 90:3509-3515.
41. Cho J., Boccaccini A.R., Shaffer M.S.P. The influence of reagent stoichiometry on the yield and aspect ratio of acid-oxidised injection CVD-grown multi-walled carbon nanotubes. Carbon 2012, 50:3967-3976.
42. Ferrari A.C., Robertson J. Interpretation of Raman spectra of disordered and amorphous carbon. Phys. Rev. B 2000, 61:14095-14107.
43. Heister E., Lamprecht C., Neves V., Tilmaciu C., Datas L., Flahaut E., et al. Higher dispersion efficacy of functionalized carbon nanotubes in chemical and biological environments. ACS Nano 2010, 4:2615-2626.
44. Pienaar I.S., Harrison I.F., Elson J.L., Bury A., Woll P., Simon A.K., et al. An animal model mimicking pedunculopontine nucleus cholinergic degeneration in Parkinson's disease. Brain Struct. Funct. 2015, 220:479-500.
45. Oberdorster E. Manufactured nanomaterials (fullerenes, C-60) induce oxidative stress in the brain of juvenile largemouth bass. Environ. Health Perspect. 2004, 112:1058-1062.
46. Liu Z., Cai W.B., He L.N., Nakayama N., Chen K., Sun X.M., et al. In vivo biodistribution and highly efficient tumour targeting of carbon nanotubes in mice. Nat. Nanotechnol. 2007, 2:47-52.
47. Belyanskaya L., Weigel S., Hirsch C., Tobler U., Krug H.F., Wick P. Effects of carbon nanotubes on primary neurons and glial cells. Neurotoxicology 2009, 30:702-711.
48. Jeong B., Park J.S., Lee K.J., Hong S.C., Hyon J.Y., Choi H., et al. Direct measurement of the force generated by a single macrophage. J. Korean Phys. Soc. 2007, 50:313-319.
49. Yu M.F., Lourie O., Dyer M.J., Moloni K., Kelly T.F., Ruoff R.S. Strength and breaking mechanism of multiwalled carbon nanotubes under tensile load. Science 2000, 287:637-640.
50. Demczyk B.G., Wang Y.M., Cumings J., Hetman M., Han W., Zettl A., et al. Direct mechanical measurement of the tensile strength and elastic modulus of multiwalled carbon nanotubes. Mater. Sci. Eng. A Struct. 2002, 334:173-178.
51. Sammalkorpi M., Krasheninnikov A., Kuronen A., Nordlund K., Kaski K. Mechanical properties of carbon nanotubes with vacancies and related defects (vol. 70, art no 245416, 2004). Phys. Rev. B 2005, 71.
52. Blighe F.M., Lyons P.E., De S., Blau W.J., Coleman J.N. On the factors controlling the mechanical properties of nanotube films. Carbon 2008, 46:41-47.
53. Lacerda L., Russier J., Pastorin G., Herrero M.A., Venturelli E., Dumortier H., et al. Translocation mechanisms of chemically functionalised carbon nanotubes across plasma membranes. Biomaterials 2012, 33:3334-3343.
54. Geng J., Kim K., Zhang J.F., Escalada A., Tunuguntla R., Comolli L.R., et al. Stochastic transport through carbon nanotubes in lipid bilayers and live cell membranes. Nature 2014, 514:612.
55. Block M.L., Zecca L., Hong J.S. Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat. Rev. Neurosci. 2007, 8:57-69.
56. Allen B.L., Kichambare P.D., Gou P., Vlasova I.I., Kapralov A.A., Konduru N., et al. Biodegradation of single-walled carbon nanotubes through enzymatic catalysis. Nano Lett. 2008, 8:3899-3903.
57. Allen B.L., Kotchey G.P., Chen Y., Yanamala N.V.K., Klein-Seetharaman J., Kagan V.E., et al. Mechanistic investigations of horseradish peroxidase-catalyzed degradation of single-walled carbon nanotubes. J. Am. Chem. Soc. 2009, 131:17194-17205.
58. Kagan V.E., Konduru N.V., Feng W., Allen B.L., Conroy J., Volkov Y., et al. Carbon nanotubes degraded by neutrophil myeloperoxidase induce less pulmonary inflammation. Nat. Nanotechnol. 2010, 5:354-359.
59. Russier J., Menard-Moyon C., Venturelli E., Gravel E., Marcolongo G., Meneghetti M., et al. Oxidative biodegradation of single- and multi-walled carbon nanotubes. Nanoscale 2011, 3:893-896.
60. Fores-Cervantes D.X., Maes H.M., Schaffer A., Hollender J., Kohler H.P.E. Slow biotransformation of carbon nanotubes by horseradish peroxidase. Environ. Sci. Technol. 2014, 48:4826-4834.
61. Kobler C., Poulsen S.S., Saber A.T., Jacobsen N.R., Wallin H., Yauk C.L., et al. Time-dependent subcellular distribution and effects of carbon nanotubes in lungs of mice. PLoS One 2015, 10.
62. Pauluhn J. Subchronic 13-week inhalation exposure of rats to multiwalled carbon nanotubes: toxic effects are determined by density of agglomerate structures, not fibrillar structures. Toxicol. Sci. 2010, 113:226-242.