Toxicity of carboxylated carbon nanotubes in endothelial cells is attenuated by stimulation of the autophagic flux with the release of nanomaterial in autophagic vesicles

Nanomedicine: Nanotechnology, Biology, and Medicine

Volumn 10, Issue 5, 2014, Pages e939-e948

  Orecna, Martina ^a   De Paoli, Silvia H ^a   Janouskova, Olga ^b,c   Tegegn, Tseday Z ^a   Filipova, Marcela ^b   Bonevich, John E ^d   Holada, Karel ^b   Simak, Jan ^a  

^a CENTER FOR BIOLOGICS EVALUATION AND RESEARCH   (United States)

^b CHARLES UNIVERSITY   (Czech Republic)

^c INSTITUTE OF MACROMOLECULAR CHEMISTRY   (Czech Republic)

^d NATIONAL INSTITUTE OF STANDARDS AND TECHNOLOGY   (United States)

Author keywords

Autophagy; Bafilomycin A1; Carbon nanotubes; Exocytosis; Microvesicles

Indexed keywords

CARBON NANOTUBES; ENDOTHELIAL CELLS; INDUSTRIAL POISONS; MEDICAL NANOTECHNOLOGY; NANOSTRUCTURED MATERIALS; TOXICITY; YARN;

AUTOPHAGY; BAFILOMYCIN; CARBOXYLATED MULTI-WALLED CARBON NANOTUBES; EXOCYTOSIS; HUMAN ENDOTHELIAL CELLS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; MICROVESICLES; SAFETY CONCERNS;

MULTIWALLED CARBON NANOTUBES (MWCN);

BAFILOMYCIN A1; CHLOROQUINE; MAMMALIAN TARGET OF RAPAMYCIN; MULTI WALLED NANOTUBE; CARBON NANOTUBE; MACROLIDE; NANOMATERIAL;

ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; BIOACCUMULATION; CELL PROTECTION; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; MEMBRANE VESICLE; MICROVESICLE; PHARMACOLOGICAL STIMULATION; UMBILICAL VEIN ENDOTHELIAL CELL; DRUG EFFECTS; ENDOTHELIUM CELL; EXOCYTOSIS; METABOLISM; PHYSIOLOGY; TOXICITY;

AUTOPHAGY; ENDOTHELIAL CELLS; EXOCYTOSIS; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MACROLIDES; NANOSTRUCTURES; NANOTUBES, CARBON;

EID: 84903521288     PISSN: 15499634     EISSN: 15499642     Source Type: Journal    
DOI: 10.1016/j.nano.2014.02.001     Document Type: Article

References (40)

1. Kostarelos K., Bianco A., Prato M. Promises, facts and challenges for carbon nanotubes in imaging and therapeutics. Nat Nanotechnol 2009, 4:627-633.
2. Gomez-Gualdron D.A., Burgos J.C., Yu J., Balbuena P.B. Carbon nanotubes: engineering biomedical applications. Prog Mol Biol Transl Sci 2011, 104:175-245.
3. De Volder M.F., Tawfick S.H., Baughman R.H., Hart A.J. Carbon nanotubes: present and future commercial applications. Science 2013, 339:535-539.
4. Choi K.Y., Liu G., Lee S., Chen X. Theranostic nanoplatforms for simultaneous cancer imaging and therapy: current approaches and future perspectives. Nanoscale 2012, 4:330-342.
5. Madani S.Y., Naderi N., Dissanayake O., Tan A., Seifalian A.M. A new era of cancer treatment: carbon nanotubes as drug delivery tools. Int J Nanomedicine 2011, 6:2963-2979.
6. Fabbro C., Ali-Boucetta H., Da Ros T., Kostarelos K., Bianco A., Prato M. Targeting carbon nanotubes against cancer. Chem Commun (Camb) 2012, 48:3911-3926.
7. Ryman-Rasmussen J.P., Cesta M.F., Brody A.R., Shipley-Phillips J.K., Everitt J.I., Tewksbury E.W., Moss O.R., Wong B.A., Dodd D.E., Andersen M.E., Bonner J.C. Inhaled carbon nanotubes reach the subpleural tissue in mice. Nat Nanotechnol 2009, 4:747-751.
8. 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.
9. 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.
10. Firme C.P., Bandaru P.R. Toxicity issues in the application of carbon nanotubes to biological systems. Nanomedicine 2010, 6:245-256.
11. Simak J. The effects of engineered nanomaterials on cultured endothelial cells. In Handbook of immunological properties of engineered nanomaterials 2013, Vol. 1:207-261. World Scientific, London. M.A. Dobrovolskaia, S.E. McNeil (Eds.).
12. Albini A., Mussi V., Parodi A., Ventura A., Principi E., Tegami S., Rocchia M., Francheschi E., Sogno I., Cammarota R., Finzi G., Sessa F., Noonan D.M., Valbusa U. Interactions of single-wall carbon nanotubes with endothelial cells. Nanomedicine 2010, 6:277-288.
13. Cheng W.W., Lin Z.Q., Ceng Q., Wei B.F., Fan X.J., Zhang H.S., Zhang W., Yang H.L., Liu H.L., Yan J., Tian L., Lin B.C., Ding S.M., Xi Z.G. Single-wall carbon nanotubes induce oxidative stress in rat aortic endothelial cells. Toxicol Mech Methods 2012, 22:268-276.
14. Cheng W.W., Lin Z.Q., Wei B.F., Zeng Q., Han B., Wei C.X., Fan X.J., Hu C.L., Liu L.H., Huang J.H., Yang X., Xi Z.G. Single-walled carbon nanotube induction of rat aortic endothelial cell apoptosis: reactive oxygen species are involved in the mitochondrial pathway. Int J Biochem Cell Biol 2011, 43:564-572.
15. Guo Y.Y., Zhang J., Zheng Y.F., Yang J., Zhu X.Q. Cytotoxic and genotoxic effects of multi-wall carbon nanotubes on human umbilical vein endothelial cells in vitro. Mutat Res 2011, 721:184-191.
16. Meng J., Han Z., Kong H., Qi X., Wang C., Xie S., Xu H. Electrospun aligned nanofibrous composite of MWCNT/polyurethane to enhance vascular endothelium cells proliferation and function. J Biomed Mater Res A 2010, 95:312-320.
17. Pacurari M., Qian Y., Fu W., Schwegler-Berry D., Ding M., Castranova V., Guo N.L. Cell permeability, migration, and reactive oxygen species induced by multiwalled carbon nanotubes in human microvascular endothelial cells. J Toxicol Environ Health A 2012, 75:129-147.
18. Vidanapathirana A.K., Lai X., Hilderbrand S.C., Pitzer J.E., Podila R., Sumner S.J., Fennell T.R., Wingard C.J., Witzmann F.A., Brown J.M. Multi-walled carbon nanotube directed gene and protein expression in cultured human aortic endothelial cells is influenced by suspension medium. Toxicology 2012, 302:114-122.
19. Walker V.G., Li Z., Hulderman T., Schwegler-Berry D., Kashon M.L., Simeonova P.P. Potential in vitro effects of carbon nanotubes on human aortic endothelial cells. Toxicol Appl Pharmacol 2009, 236:319-328.
20. Choi A.M., Ryter S.W., Levine B. Autophagy in human health and disease. N Engl J Med 2013, 368:651-662.
21. Kuballa P., Nolte W.M., Castoreno A.B., Xavier R.J. Autophagy and the immune system. Annu Rev Immunol 2012, 30:611-646.
22. Stern S.T., Adiseshaiah P.P., Crist R.M. Autophagy and lysosomal dysfunction as emerging mechanisms of nanomaterial toxicity. Part Fibre Toxicol 2012, 9:20.
23. 2+ influx sensitive to calcium entry inhibitors. Nano Lett 2009, 9:3312-3317.
24. Lacerda S.H., 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.
25. Gelderman M.P., Simakova O., Clogston J.D., Patri A.K., Siddiqui S.F., Vostal A.C., Simak J. Adverse effects of fullerenes on endothelial cells: fullerenol C60(OH)24 induced tissue factor and ICAM-I membrane expression and apoptosis in vitro. Int J Nanomedicine 2008, 3:59-68.
26. Simak J., Holada K., D'agnillo F., Janota J., Vostal J.G. Cellular prion protein is expressed on endothelial cells and is released during apoptosis on membrane microparticles found in human plasma. Transfusion 2002, 42:334-342.
27. Ma X., Wu Y., Jin S., Tian Y., Zhang X., Zhao Y., Yu L., Liang X.J. Gold nanoparticles induce autophagosome accumulation through size-dependent nanoparticle uptake and lysosome impairment. ACS Nano 2011, 5:8629-8639.
28. Pivtoraiko V.N., Harrington A.J., Mader B.J., Luker A.M., Caldwell G.A., Caldwell K.A., Roth K.A., Shacka J.J. Low-dose bafilomycin attenuates neuronal cell death associated with autophagy-lysosome pathway dysfunction. J Neurochem 2010, 114:1193-1204.
29. Gelderman M.P., Simak J. Flow cytometric analysis of cell membrane microparticles. Methods Mol Biol 2008, 484:79-93.
30. Morchang A., Yasamut U., Netsawang J., Noisakran S., Wongwiwat W., Songprakhon P., Srisawat C., Puttikhunt C., Kasinrerk W., Malasit P., Yenchitsomanus P.T., Limjindaporn T. Cell death gene expression profile: role of RIPK2 in dengue virus-mediated apoptosis. Virus Res 2011, 156:25-34.
31. Shacka J.J., Klocke B.J., Roth K.A. Autophagy, bafilomycin and cell death: the "a-B-cs" of plecomacrolide-induced neuroprotection. Autophagy 2006, 2:228-230.
32. Shacka J.J., Klocke B.J., Shibata M., Uchiyama Y., Datta G., Schmidt R.E., Roth K.A. Bafilomycin A1 inhibits chloroquine-induced death of cerebellar granule neurons. Mol Pharmacol 2006, 69:1125-1136.
33. Tsvetkov A.S., Miller J., Arrasate M., Wong J.S., Pleiss M.A., Finkbeiner S. A small-molecule scaffold induces autophagy in primary neurons and protects against toxicity in a Huntington disease model. Proc Natl Acad Sci U S A 2010, 107:16982-16987.
34. Ishida Y., Yamamoto A., Kitamura A., Lamande S.R., Yoshimori T., Bateman J.F., Kubota H., Nagata K. Autophagic elimination of misfolded procollagen aggregates in the endoplasmic reticulum as a means of cell protection. Mol Biol Cell 2009, 20:2744-2754.
35. 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.
36. Nixon R.A. Autophagy, amyloidogenesis and Alzheimer disease. J Cell Sci 2007, 120:4081-4091.
37. Pallet N., Sirois I., Bell C., Hanafi L.A., Hamelin K., Dieude M., Rondeau C., Thibault P., Desjardins M., Hebert M.J. A comprehensive characterization of membrane vesicles released by autophagic human endothelial cells. Proteomics 2013, 13:1108-1120.
38. Sirois I., Groleau J., Pallet N., Brassard N., Hamelin K., Londono I., Pshezhetsky A.V., Bendayan M., Hebert M.J. Caspase activation regulates the extracellular export of autophagic vacuoles. Autophagy 2012, 8:927-937.
39. Duran J.M., Anjard C., Stefan C., Loomis W.F., Malhotra V. Unconventional secretion of Acb1 is mediated by autophagosomes. J Cell Biol 2010, 188:527-536.
40. Manjithaya R., Anjard C., Loomis W.F., Subramani S. Unconventional secretion of Pichia pastoris Acb1 is dependent on GRASP protein, peroxisomal functions, and autophagosome formation. J Cell Biol 2010, 188:537-546.