Hemotoxicity of carbon nanotubes

Advanced Drug Delivery Reviews

Volumn 65, Issue 15, 2013, Pages 2127-2134

  Bussy, Cyrill ^a   Methven, Laura ^a,b   Kostarelos, Kostas ^a  

^a UNIVERSITY OF MANCHESTER   (United Kingdom)

^b KING S COLLEGE HOSPITAL   (United Kingdom)

Author keywords

Blood; Coagulation; Complement; Hemocompatibility; Multi walled carbon nanotubes; Nanotoxicology; Single walled carbon nanotubes; Thrombosis

Indexed keywords

BIOMEDICAL APPLICATIONS; CIRCULATORY SYSTEMS; COMPLEMENT; COMPLEMENT SYSTEMS; HEMOCOMPATIBILITY; NANOTOXICOLOGY; SYSTEMIC CIRCULATION; THROMBOSIS;

BLOOD; COAGULATION; MEDICAL APPLICATIONS; MULTIWALLED CARBON NANOTUBES (MWCN); RISK ASSESSMENT; SINGLE-WALLED CARBON NANOTUBES (SWCN);

PROTEINS;

CAPROLACTAM; CARBON NANOTUBE; FIBRINOGEN; IMMUNOGLOBULIN; KETOCONAZOLE; MULTI WALLED NANOTUBE; PHOSPHOLIPASE C; PLASMA PROTEIN; PROTEIN KINASE C; SINGLE WALLED NANOTUBE;

BLOOD CLOTTING; BLOOD COMPATIBILITY; BLOOD TOXICITY; CALCIUM SIGNALING; COMPLEMENT ACTIVATION; COMPLEMENT CLASSICAL PATHWAY; COMPLEMENT SYSTEM; ERYTHROCYTE; HEMOLYSIS; HEMOSTASIS; HUMAN; LEUKOCYTE; NANOMEDICINE; NONHUMAN; PLASMA PROTEIN BINDING; PRIORITY JOURNAL; PROTEIN INTERACTION; RETICULOCYTE; REVIEW; RISK ASSESSMENT; THROMBOCYTE ACTIVATION; THROMBOCYTE AGGREGATION;

BLOOD; COAGULATION; COMPLEMENT; HEMOCOMPATIBILITY; MULTI-WALLED CARBON NANOTUBES; NANOTOXICOLOGY; SINGLE WALLED CARBON NANOTUBES; THROMBOSIS;

ANIMALS; BLOOD PROTEINS; COMPLEMENT SYSTEM PROTEINS; ENVIRONMENTAL EXPOSURE; ERYTHROCYTES; HEMOSTASIS; HUMANS; NANOTUBES, CARBON; RISK ASSESSMENT;

EID: 84888872343     PISSN: 0169409X     EISSN: 18728294     Source Type: Journal    
DOI: 10.1016/j.addr.2013.10.008     Document Type: Review

References (65)

1. Iijima S. Helical microtubules of graphitic carbon. Nature 1991, 354:56-58.
2. Lu W.B., Zu M., Byun J.H., Kim B.S., Chou T.W. State of the art of carbon nanotube fibers: opportunities and challenges. Adv. Mater. 2012, 24:1805-1833.
3. Tasis D., Tagmatarchis N., Bianco A., Prato M. Chemistry of carbon nanotubes. Chem. Rev. 2006, 106:1105-1136.
4. Zamolo V., Vazquez E., Prato M. Carbon Nanotubes: Synthesis, Structure, Functionalization, and Characterization 2013, 1-45. Springer, Berlin Heidelberg.
5. De Volder M.F.L., Tawfick S.H., Baughman R.H., Hart A.J. Carbon nanotubes: present and future commercial applications. Science 2013, 339:535-539.
6. Menard-Moyon C., Kostarelos K., Prato M., Bianco A. Functionalized carbon nanotubes for probing and modulating molecular functions. Chem. Biol. 2010, 17:107-115.
7. Barone P.W., Baik S., Heller D.A., Strano M.S. Near-infrared optical sensors based on single-walled carbon nanotubes. Nat. Mater. 2005, 4:86-92.
8. Nayak T.R., Jian L., Phua L.C., Ho H.K., Ren Y.P., Pastorin G. Thin films of functionalized multiwalled carbon nanotubes as suitable scaffold materials for stem cells proliferation and bone formation. ACS Nano 2010, 4:7717-7725.
9. Wang L., Shi J., Zhang H., Li H., Gao Y., Wang Z., Wang H., Li L., Zhang C., Chen C., Zhang Z., Zhang Y. Synergistic anticancer effect of RNAi and photothermal therapy mediated by functionalized single-walled carbon nanotubes. Biomaterials 2013, 34:262-274.
10. Murakami T., Nakatsuji H., Inada M., Matoba Y., Umeyama T., Tsujimoto M., Isoda S., Hashida M., Imahori H. Photodynamic and photothermal effects of semiconducting and metallic-enriched single-walled carbon nanotubes. J. Am. Chem. Soc. 2012, 134:17862-17865.
11. Kim J.W., Galanzha E.I., Shashkov E.V., Moon H.M., Zharov V.P. Golden carbon nanotubes as multimodal photoacoustic and photothermal high-contrast molecular agents. Nat. Nanotechnol. 2009, 4:688-694.
12. De la Zerda A., Kim J.W., Galanzha E.I., Gambhir S.S., Zharov V.P. Advanced contrast nanoagents for photoacoustic molecular imaging, cytometry, blood test and photothermal theranostics. Contrast Media Mol. Imaging 2011, 6:346-369.
13. Robinson J.T., Hong G., Liang Y., Zhang B., Yaghi O.K., Dai H. In vivo fluorescence imaging in the second near-infrared window with long circulating carbon nanotubes capable of ultrahigh tumor uptake. J. Am. Chem. Soc. 2012, 134:10664-10669.
14. Hong G., Lee J.C., Robinson J.T., Raaz U., Xie L., Huang N.F., Cooke J.P., Dai H. Multifunctional in vivo vascular imaging using near-infrared II fluorescence. Nat. Med. 2012, 18:1841-1846.
15. Delogu L.G., Vidili G., Venturelli E., Menard-Moyon C., Zoroddu M.A., Pilo G., Nicolussi P., Ligios C., Bedognetti D., Sgarrella F., Manetti R., Bianco A. Functionalized multiwalled carbon nanotubes as ultrasound contrast agents. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:16612-16617.
16. Bianco A., Kostarelos K., Prato M. Applications of carbon nanotubes in drug delivery. Curr. Opin. Chem. Biol. 2005, 9:674-679.
17. Kostarelos K., Bianco A., Prato M. Promises, facts and challenges for carbon nanotubes in imaging and therapeutics. Nat. Nanotechnol. 2009, 4:627-633.
18. 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.
19. Donaldson K., Murphy F.A., Duffin R., Poland C.A. Asbestos, carbon nanotubes and the pleural mesothelium: a review of the hypothesis regarding the role of long fibre retention in the parietal pleura, inflammation and mesothelioma. Part. Fibre Toxicol. 2010, 7:5.
20. 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.
21. Boczkowski J., Lanone S. Respiratory toxicities of nanomaterials - a focus on carbon nanotubes. Adv. Drug Deliv. Rev. 2012, 64:1694-1699.
22. Shvedova A.A., Kisin E.R., Porter D., Schulte P., Kagan V.E., Fadeel B., Castranova V. Mechanisms of pulmonary toxicity and medical applications of carbon nanotubes: two faces of Janus?. Pharmacol. Ther. 2009, 121:192-204.
23. Ratner B.D., Hoffman A.S., Schoen F.J., Lemons J.E. Biomaterials Science, an Introduction to Materials in Medicine 2012, Academic Press. Third ed.
24. Zipfel P.F., Skerka C. Complement regulators and inhibitory proteins. Nat. Rev. Immunol. 2009, 9:729-740.
25. Harboe M., Thorgersen E.B., Mollnes T.E. Advances in assay of complement function and activation. Adv. Drug Deliv. Rev. 2011, 63:976-987.
26. Szebeni J., Alving C.R., Rosivall L., Bunger R., Baranyi L., Bedocs P., Toth M., Barenholz Y. Animal models of complement-mediated hypersensitivity reactions to liposomes and other lipid-based nanoparticles. J. Liposome. Res. 2007, 17:107-117.
27. Engelmann B., Massberg S. Thrombosis as an intravascular effector of innate immunity. Nat. Rev. Immunol. 2013, 13:34-45.
28. Dobrovolskaia M.A., Germolec D.R., Weaver J.L. Evaluation of nanoparticle immunotoxicity. Nat. Nanotechnol. 2009, 4:411-414.
29. Casals E., Puntes V.F. Inorganic nanoparticle biomolecular corona: formation, evolution and biological impact. Nanomedicine (Lond) 2012, 7:1917-1930.
30. Karakoti A.S., Das S., Thevuthasan S., Seal S. PEGylated inorganic nanoparticles. Angew. Chem. Int. Ed. Engl. 2011, 50:1980-1994.
31. Monopoli M.P., Aberg C., Salvati A., Dawson K.A. Biomolecular coronas provide the biological identity of nanosized materials. Nat. Nanotechnol. 2012, 7:779-786.
32. Fadeel B. Clear and present danger? Engineered nanoparticles and the immune system. Swiss Med. Wkly. 2012, 142:w13609.
33. Walkey C.D., Chan W.C. Understanding and controlling the interaction of nanomaterials with proteins in a physiological environment. Chem. Soc. Rev. 2012, 41:2780-2799.
34. Bianco A., Kostarelos K., Partidos C.D., Prato M. Biomedical applications of functionalised carbon nanotubes. Chem. Commun. 2005, 571-577.
35. Herrero M.A., Lacerda L., Bianco A., Kostarelos K., Prato M. Functionalised carbon nanotubes: high biocompatibility with lack of toxicity. Int. J. Nanotechnol. 2011, 8:885-897.
36. Prato M., Kostarelos K., Bianco A. Functionalized carbon nanotubes in drug design and discovery. Acc. Chem. Res. 2008, 41:60-68.
37. Lanone S., Andujar P., Kermanizadeh A., Boczkowski J. Determinants of carbon nanotube toxicity. Adv. Drug Deliv. Rev. 2013, 10.1016/j.addr.2013.07.019.
38. Salvador-Morales C., Flahaut E., Sim E., Sloan J., Green M.L., Sim R.B. Complement activation and protein adsorption by carbon nanotubes. Mol. Immunol. 2006, 43:193-201.
39. Salvador-Morales C., Basiuk E.V., Basiuk V.A., Green M.L., Sim R.B. Effects of covalent functionalization on the biocompatibility characteristics of multi-walled carbon nanotubes. J. Nanosci. Nanotechnol. 2008, 8:2347-2356.
40. Ge C., Du J., Zhao L., Wang L., Liu Y., Li D., Yang Y., Zhou R., Zhao Y., Chai Z., Chen C. Binding of blood proteins to carbon nanotubes reduces cytotoxicity. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:16968-16973.
41. Sacchetti C., Motamedchaboki K., Magrini A., Palmieri G., Mattei M., Bernardini S., Rosato N., Bottini N., Bottini M. Surface polyethylene glycol conformation influences the protein corona of polyethylene glycol-modified single-walled carbon nanotubes: potential implications on biological performance. ACS Nano 2013, 7:1974-1989.
42. Rybak-Smith M.J., Sim R.B. Complement activation by carbon nanotubes. Adv. Drug Deliv. Rev. 2011, 63:1031-1041.
43. Ling W.L., Biro A., Bally I., Tacnet P., Deniaud A., Doris E., Frachet P., Schoehn G., Pebay-Peyroula E., Arlaud G.J. Proteins of the innate immune system crystallize on carbon nanotubes but are not activated. ACS Nano 2011, 5:730-737.
44. Hamad I., Christy Hunter A., Rutt K.J., Liu Z., Dai H., Moein Moghimi S. Complement activation by PEGylated single-walled carbon nanotubes is independent of C1q and alternative pathway turnover. Mol. Immunol. 2008, 45:3797-3803.
45. Andersen A.J., Robinson J.T., Dai H., Hunter A.C., Andresen T.L., Moghimi S.M. Single-walled carbon nanotube surface control of complement recognition and activation. ACS Nano 2013, 7:1108-1119.
46. Andersen A.J., Windschiegl B., Ilbasmis-Tamer S., Degim I.T., Hunter A.C., Andresen T.L., Moghimi S.M. Complement activation by PEG-functionalized multi-walled carbon nanotubes is independent of PEG molecular mass and surface density. Nanomed. Nanotechnol. Biol. Med. 2013, 9:469-473.
47. Donkor A.D., Su Z.D., Mandal H.S., Jin X., Tang X.W. Carbon nanotubes inhibit the hemolytic activity of the pore-forming toxin pyolysin. Nano Res. 2009, 2:517-525.
48. Sachar S., Saxena R.K. Cytotoxic effect of poly-dispersed single walled carbon nanotubes on erythrocytes in vitro and in vivo. PLoS One 2011, 6:e22032.
49. Meng J., Cheng X.L., Liu J., Zhang W.Q., Li X.J., Kong H., Xu H.Y. Effects of long and short carboxylated or aminated multiwalled carbon nanotubes on blood coagulation. PLoS One 2012, 7:e38995.
50. Guo M., Li D., Zhao M., Zhang Y., Deng X., Geng D., Li R., Sun X., Gu H., Wan R. NH2+ implantations induced superior hemocompatibility of carbon nanotubes. Nanoscale Res. Lett. 2013, 8:205.
51. Radomski A., Jurasz P., Alonso-Escolano D., Drews M., Morandi M., Malinski T., Radomski M.W. Nanoparticle-induced platelet aggregation and vascular thrombosis. Br. J. Pharmacol. 2005, 146:882-893.
52. Bihari P., Holzer M., Praetner M., Fent J., Lerchenberger M., Reichel C.A., Rehberg M., Lakatos S., Krombach F. Single-walled carbon nanotubes activate platelets and accelerate thrombus formation in the microcirculation. Toxicology 2010, 269:148-154.
53. 2+ influx sensitive to calcium entry inhibitors. Nano Lett. 2009, 9:3312-3317.
54. Lacerda S.H.D., Semberova J., Holada K., Simakova O., Hudson S.D., Simak J. Carbon nanotubes activate store-operated calcium entry in human blood platelets. ACS Nano 2011, 5:5808-5813.
55. Guidetti G.F., Consonni A., Cipolla L., Mustarelli P., Balduini C., Torti M. Nanoparticles induce platelet activation in vitro through stimulation of canonical signalling pathways. Nanomed. Nanotechnol 2012, 8:1329-1336.
56. Burke A.R., Singh R.N., Carroll D.L., Owen J.D., Kock N.D., D'Agostino R., Torti F.M., Torti S.V. Determinants of the thrombogenic potential of multiwalled carbon nanotubes. Biomaterials 2011, 32:5970-5978.
57. Vakhrusheva T.V., Gusev A.A., Gusev S.A., Vlasova I.I. Albumin reduces thrombogenic potential of single-walled carbon nanotubes. Toxicol. Lett. 2013, 221:137-145.
58. Zolnik B.S., Gonzalez-Fernandez A., Sadrieh N., Dobrovolskaia M.A. Nanoparticles and the immune system. Endocrinology 2010, 151:458-465.
59. Neun B.W., Dobrovolskaia M.A. Qualitative analysis of total complement activation by nanoparticles. Methods Mol. Biol. 2011, 697:237-245.
60. Neun B.W., Dobrovolskaia M.A. Method for in vitro analysis of nanoparticle thrombogenic properties. Methods Mol. Biol. 2011, 697:225-235.
61. Neun B.W., Dobrovolskaia M.A. Method for analysis of nanoparticle hemolytic properties in vitro. Methods Mol. Biol. 2011, 697:215-224.
62. Ali-Boucetta H., Nunes A., Sainz R., Herrero M.A., Tian B.W., Prato M., Bianco A., Kostarelos K. Asbestos-like pathogenicity of long carbon nanotubes alleviated by chemical functionalization. Angew. Chem. Int. Edit. 2013, 52:2274-2278.
63. Bussy C., Pinault M., Cambedouzou J., Landry M.J., Jegou P., Mayne-L'hermite M., Launois P., Boczkowski J., Lanone S. Critical role of surface chemical modifications induced by length shortening on multi-walled carbon nanotubes-induced toxicity. Part. Fibre. Toxicol. 2012, 9:46.
64. Kostarelos K., Lacerda L., Pastorin G., Wu W., Wieckowski S., Luangsivilay J., Godefroy S., Pantarotto D., Briand J.P., Muller S., Prato M., Bianco A. Cellular uptake of functionalized carbon nanotubes is independent of functional group and cell type. Nat. Nanotechnol. 2007, 2:108-113.
65. Bianco A., Kostarelos K., Prato M. Making carbon nanotubes biocompatible and biodegradable. Chem. Commun. 2011, 47:10182-10188.