Silica nanoparticle uptake induces survival mechanism in A549 cells by the activation of autophagy but not apoptosis

Toxicology Letters

Volumn 224, Issue 1, 2014, Pages 84-92

  Nowak, Jakub Stanislaw ^a   Mehn, Dora ^a   Nativo, Paola ^a   García, César Pascual ^a   Gioria, Sabrina ^a   Ojea Jiménez, Isaac ^a   Gilliland, Douglas ^a   Rossi, François ^a  

^a JOINT RESEARCH CENTRE   (Italy)

Author keywords

A549; Autophagy; Cytotoxicity; Nanoparticle; Silica

Indexed keywords

CASPASE 3; CASPASE 8; CASPASE 9; COPPER ZINC SUPEROXIDE DISMUTASE; CYCLOOXYGENASE 2; CYTOCHROME C'; GLUTATHIONE PEROXIDASE 1; INDUCIBLE NITRIC OXIDE SYNTHASE; NANOPARTICLE; PLASMA PROTEIN; SILICON DIOXIDE; TRANSCRIPTION FACTOR NRF2;

APOPTOSIS; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY; CELL STRUCTURE; CELL SURVIVAL; CYTOKINE RELEASE; CYTOTOXICITY; FLUORESCENCE MICROSCOPY; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; LUNG ALVEOLUS EPITHELIUM; PINOCYTOSIS; PRIORITY JOURNAL; SCANNING ELECTRON MICROSCOPY; TRANSMISSION ELECTRON MICROSCOPY; ZETA POTENTIAL;

A549; AUTOPHAGY; CYTOTOXICITY; NANOPARTICLE; SILICA;

APOPTOSIS; AUTOPHAGY; CELL LINE, TUMOR; CELL SURVIVAL; HUMANS; NANOPARTICLES; SILICON DIOXIDE;

EID: 84887547893     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2013.10.003     Document Type: Article

References (48)

1. Bagwe P., Hilliard L.R., Tan W. Surface modification of silica nanoparticles to reduce aggregation and nonspecific binding. Langmuir 2006, 22:4357-4362.
2. Beau I., Mehrpour M., Codogno P. Autophagosomes and human diseases. Int. J. Biochem. Cell. Biol. 2011, 43:460-464.
3. Biederbick A., Kern H.F., Elsasser H.P. Monodansylcadaverine (MDC) is a specific in vivo marker for autophagic vacuoles. Eur. J. Cell. Biol. 1995, 66:3-14.
4. Cho E.C., Xie J., Wurm P.A., Xia Y. Understanding the role of surface charges in cellular adsorption versus internalization by selectively removing gold nanoparticles on the cell surface with a I2/KI etchant. Nano Lett. 2009, 9:1080-1084.
5. Choi S.J., Oh J.M., Choy J.H. Toxicological effects of inorganic nanoparticles on human lung cancer A549 cells. J. Inorg. Biochem. 2009, 103:463-471.
6. del Campo A., Sena T., Lellouchec J.P., Brucea I.J. Multifunctional magnetite and silica-magnetite nanoparticles: synthesis, surface activation and applications in life sciences. J. Magn. Magn. Mater. 2005, 293:33-40.
7. Deveraux Q.L., Roy N., Stennicke H.R., Van Arsdale T., Zhou Q., Srinivasula S.M., Alnemri E.S., Salvesen G.S., Reed J.C. IAPs block apoptotic events induced by caspase-8 and cytochrome c by direct inhibition of distinct caspases. EMBO J. 1998, 17:2215-2223.
8. Fanizza C., Fresegna A.M., Maiello R., Paba E., Cavallo D. Evaluation of cytotoxic concentration-time response in A549 cells exposed to respirable α-quartz. J. Appl. Toxicol. 2009, 29:537-544.
9. Geiser M., Casaulta M., Kupferschmid B., Schulz H., Semmler-Behnke M., Kreyling W. The role of macrophages in the clearance of inhaled ultrafine titanium dioxide particles. Am. J. Respir. Cell. Mol. Biol. 2008, 38:371-376.
10. Hartlen K.D., Athanasopoulos A.P.T., Kitaev V. Facile preparation of highly monodisperse small silica spheres (15->200nm) suitable for colloidal templating and formation of ordered arrays. Langmuir 2008, 1714-1720.
11. He Q., Zhang Z., Gao Y., Shi J., Li Y. Intracellular localization and cytotoxicity of spherical mesoporous silica nano- and microparticles. Small 2009, 5:2722-2729.
12. Herd H.L., Malugin A., Ghandehari H. Silica nanoconstruct cellular toleration threshold in vitro. J. Control. Release 2011, 153:40-48.
13. Isoda K., Hasezaki T., Kondoh M., Tsutsumi Y., Yagi K. Effect of surface charge on nano-sized silica particles-induced liver injury. Pharmazie 2011, 278-281.
14. Jin Y., Kannan S., Wu M., Zhao J.X. Toxicity of luminescent silica nanoparticles to living cells. Chem. Res. Toxicol. 2007, 20:1126-1133.
15. Jung C.H., Ro S.-H., Cao J., Otto N.M., Kim D.-H. mTOR regulation of autophagy. FEBS Lett. 2010, 584:1287-1295.
16. Li J.J., Muralikrishnan S., Ng Ch.T., Yung L-Y.L., Bay B.-H. Nanoparticle-induced pulmonary toxicity. Exp. Biol. Med. 2010, 235:1025-1033.
17. Lieber M., Smith B., Szakal A., Nelson-Rees W., Todaro G. A continuous tumor-cell line from a human lung carcinoma with properties of type II alveolar epithelial cells. Int. J. Cancer 1976, 17:62-70.
18. Lin W., Huang Y.W., Zhou X.D., Ma Y. In vitro toxicity of silica nanoparticles in human lung cancer cells. Toxicol. Appl. Pharmacol. 2006, 217:252-259.
19. Liong M., Lu J., Kovochich M., Xia T., Ruehm S.G., Nel A.E., Tamanoi F., Zink J.I. Multifunctional inorganic nanoparticles for imaging, targeting, and drug delivery. ACS Nano 2008, 889-896.
20. Lu X., Qian J., Zhou H., Gan Q., Tang W., Lu J., Yuan Y., Liu C. In vitro cytotoxicity and induction of apoptosis by silica nanoparticles in human HepG2 hepatoma cells. Int. J. Nanomed. 2011, 6:1889-1901.
21. Macia E., Ehrlich M., Massol R., Boucrot E., Brunner C., Kirchhausen T. Dynasore, a cell-permeable inhibitor of dynamin. Dev. Cell 2006, 10:839-850.
22. McCormick J., Knight R.A., Barry S.P., Scarabelli T.M., Abounit K., Latchman D.S., Stephanou A. Autophagy in the stress-induced myocardium. Front. Biosci. 2012, 4:2131-2141.
23. Meng H., Yang S., Li Z., Xia T., Chen J., Ji Z., Zhang H., Wang X., Lin S., Huang C., Zhou Z.H., Zink J.I., Nel A.E. Aspect ratio determines the quantity of mesoporous silica nanoparticle uptake by a small GTPase-dependent macropinocytosis mechanism. ACS Nano 2011, 5:4434-4447.
24. Motadi L.R., Misso N.L., Dlamini Z., Bhoola K.D. Molecular genetics and mechanisms of apoptosis in carcinomas of the lung and pleura: therapeutic targets. Int. Immunopharmacol. 2007, 7:1934-1947.
25. Napierska D., Thomassen L.C., Rabolli V., Lison D., Gonzalez L., Kirsch-Volders M., Martens J.A., Hoet P.H. Size-dependent cytotoxicity of monodisperse silica nanoparticles in human endothelial cells. Small 2009, 5:846-853.
26. Napierska D., Thomassen L.C., Lison D., Martens J.A., Hoet P.H. The nanosilica hazard: another variable entity. Part. Fibre Toxicol. 2010, 7:39.
27. Nieminen A.L., Gores G.J., Bond J.M., Imberti R., Herman B., Lemasters J.J. A novel cytotoxicity screening assay using a multiwell fluorescence scanner. Toxicol. Appl. Pharmacol. 1992, 115:147-155.
28. Oberdörster G. Pulmonary effects of inhaled ultrafine particles. Int. Arch. Occup. Environ. Health 2001, 74:1-8.
29. Park S., Lee Y.K., Jung M., Kim K.H., Chung N., Ahn E.K., Lim Y., Lee K.H. Cellular toxicity of various inhalable metal nanoparticles on human alveolar epithelial cells. Inhal. Toxicol. 2007, 19(Suppl. 1):59-65.
30. Paget V., Sergent J.A., Chevillard S. Nano-silicon dioxide toxicological characterization on two human kidney cell lines. J. Phys.: Conf. Ser. 2011, 304:01208.
31. Ravi Kumar M.N., Sameti M., Mohapatra S.S., Kong X., Lockey R.F., Bakowsky U., Lindenblatt G., Schmidt H., Lehr C.M. Cationic silica nanoparticles as gene carriers: synthesis, characterization and transfection efficiency in vitro and in vivo. J. Nanosci. Nanotechnol. 2004, 4:876-881.
32. Rosenholm J.M., Sahlgren C., Lindén M. Towards multifunctional, targeted drug delivery systems using mesoporous silica nanoparticles-opportunities & challenges. Nanoscale 2010, 2:1870-1883.
33. Salvati A., Pitek A.S., Monopoli M.P., Prapainop K., Baldelli Bombelli F., Hristov D.R., Kelly Ph.K., Åberg Ch., Mahon E., Dawson K.A. Transferrin-functionalized nanoparticles lose their targeting capabilities when a biomolecule corona adsorbs on the surface. Nat. Nanotechnol. 2013, 8:137-143.
34. Sandvig K., Torgersen M.L., Andersen R., van Deurs B. Clathrin-independent endocytosis: from nonexisting to an extreme degree of complexity. Histochem. Cell. Biol. 2008, 129:267-276.
35. Schweichel J.U., Merker H.J. The morphology of various types of cell death in prenatal tissues. Teratology 1973, 7:253-266.
36. Sharma P., Brown S., Walter G., Santra S., Moudgil B. Particle Nanoparticles for bioimaging. Adv. Colloid. Interface Sci. 2006, 123-126:471-485.
37. 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 2008, 253:137-146.
38. Singh K., Matsuyama S., Drazba J.A., Almasan A. Autophagy-dependent senescence in response to DNA damage and chronic apoptotic stress. Autophagy 2012, 8:236-251.
39. Stearns R.C., Paulauskis J.D., Godlesk J.J. Endocytosis of ultrafine particles by A549 cells. Am. J. Respir. Cell. Mol. Biol. 2001, 24:108-115.
40. 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.
41. 2 nanoparticles induce cytotoxicity and protein expression alteration in HaCaT cells. J. Appl. Toxicol. Part. Fibre Toxicol. 2010, 7:1.
42. Yu T., Malugin A., Ghandehari H. Impact of silica nanoparticle design on cellular toxicity and hemolytic activity. ACS Nano 2011, 5:5717-5728.
43. Ye Y., Liu J., Chen M., Sun L., Lan M. In vitro toxicity of silica nanoparticles in myocardial cells. Environ. Toxicol. Pharmacol. 2010, 29:131-137.
44. Yokoi T., Sakamoto Y., Terasaki O., Kubota Y., Okubo T., Tatsumi T. Periodic arrangement of silica nanospheres assisted by amino acids. J. Am. Chem. Soc. 2006, 128:13664-21366.
45. Wang F., Gao F., Lan M., Yuan H., Huang Y., Liu J. Oxidative stress contributes to silica nanoparticle-induced cytotoxicity in human embryonic kidney cells. Toxicol. In Vitro 2009, 23:808-815.
46. Wang P., Guan Y.-F., Du H., Zhai Q.-W., Su D.-F., Miao C.-Y. Induction of autophagy contributes to the neuroprotection of nicotinamide phosphoribosyltransferase in cerebral ischemia. Autophagy 2012, 77-87.
47. Waters K.M., Masiello L.M., Zangar R.C., Tarasevich B.J., Karin N.J., Quesenberry R.D., Bandyopadhyay S., Teeguarden J.G., Pounds J.G., Thrall B.D. Macrophage responses to silica nanoparticles are highly conserved across particle sizes. Toxicol. Sci. 2009, 107:553-569.
48. Zhivotovsky B., Orrenius S. Cell death mechanisms: cross-talk and role in disease. Exp. Cell. Res. 2010, 316:1374-1383.