Autophagy induction by silver nanowires: A new aspect in the biocompatibility assessment of nanocomposite thin films

Toxicology and Applied Pharmacology

Volumn 264, Issue 3, 2012, Pages 451-461

  Verma, Navin K ^a   Conroy, Jennifer ^a   Lyons, Philip E ^a   Coleman, Jonathan ^a   O'Sullivan, Mary P ^a   Kornfeld, Hardy ^b   Kelleher, Dermot ^a   Volkov, Yuri ^a  

^a TRINITY COLLEGE DUBLIN   (Ireland)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

Autophagy; Biohazard assessment; Cytotoxicity; Silver nanowire (AgNW)

Indexed keywords

MICROTUBULE ASSOCIATED PROTEIN; MICROTUBULE ASSOCIATED PROTEIN LIGHT CHAIN 3; NANOCOMPOSITE; NANOWIRE; SILVER; SILVER NANOWIRE; UNCLASSIFIED DRUG;

ARTICLE; ATOMIC FORCE MICROSCOPY; AUTOPHAGOSOME; AUTOPHAGY; BIOCOMPATIBILITY; BIOSAFETY; CELL LINE; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; ENDOTHELIUM CELL; EPITHELIUM CELL; FILM; HOMEOSTASIS; HUMAN; HUMAN CELL; IMAGE ANALYSIS; IMPEDANCE; PHAGOCYTE; PROTEIN AGGREGATION; TRANSMISSION ELECTRON MICROSCOPY; WESTERN BLOTTING;

ANIMALS; AUTOPHAGY; BIOCOMPATIBLE MATERIALS; BLOTTING, WESTERN; CELL LINE; HUMANS; MICE; MICROSCOPY, ELECTRON, TRANSMISSION; NANOCOMPOSITES; NANOWIRES; SILVER;

EID: 84867859391     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2012.08.023     Document Type: Article

References (82)

1. Baehrecke E.H. Autophagy: dual roles in life and death?. Nat. Rev. Mol. Cell Biol. 2005, 6:505-510.
2. Byrne F., Prina-Mello A., Whelan A., Mohamed B.M., Davies A., Gun'ko Y.K., Coey J.M.D., Volkov Y. High content analysis of the biocompatibility of nickel nanowires. J. Magn. Magn. Mater. 2009, 321:1341-1345.
3. Chen Y., Yang L., Feng C., Wen L.P. Nano neodymium oxide induces massive vacuolization and autophagic cell death in non-small cell lung cancer NCI-H460 cells. Biochem. Biophys. Res. Commun. 2005, 337:52-60.
4. Chen J., Hessler J.A., Putchakayala K., Panama B.K., Khan D.P., Hong S., Mullen D.G., DiMaggio S.C., Som A., Tew G.N., Lopatin A.N., Baker J.R., Holl M.M.B., Orr B.G. Cationic nanoparticles induce nanoscale disruption in living cell plasma membrane. J. Phys. Chem. 2009, 113:11179-11185.
5. Cortese-Krott M.M., Münchow M., Pirev E., Hessner F., Bozkurt A., Uciechowski P., Pallua N., Kröncke K.D., Suschek C.V. Silver ions induce oxidative stress and intracellular zinc release in human skin fibroblasts. Free Radic. Biol. Med. 2009, 47:1570-1577.
6. De S., Higgins T.M., Lyons P.E., Doherty E.M., Nirmalraj P.N., Blau W.J., Boland J.J., Coleman J.N. Silver nanowire networks as flexible, transparent, conducting films: extremely high DC to optical conductivity ratios. ACS Nano 2009, 3:1767-1774.
7. Deretic V. Autophagy in infection. Curr. Opin. Cell Biol. 2010, 22:252-262.
8. Foldbjerg R., Dang D.A., Autrup H. Cytotoxicity and genotoxicity of silver nanoparticles in the human lung cancer cell line, A549. Arch. Toxicol. 2011, 85:743-750.
9. Franz C.M., Puech P.H. Atomic force microscope: a versatile tool for studying cell morphology, adhesion and mechanics. Cell. Mol. Bioeng. 2008, 1:289-300.
10. Gaczynska M., Osmulski P.A. AFM of biological complexes: what can we learn?. Curr. Opin. Colloid 2008, 13:351-367.
11. Harris J., Hartman M., Roche C., Zeng S.G., O'Shea A., Sharp F.A., Lambe E.M., Creagh E.M., Golenbock D.T., Tschopp J., Kornfeld H., Fitzgerald K.A., Lavelle E.C. Autophagy controls IL-1β secretion by targeting pro-IL-1β for degradation. J. Biol. Chem. 2011, 286:9587-9597.
12. Hartman M.L., Kornfeld H. Interactions between naïve and infected macrophages reduce Mycobacterium tuberculosis viability. PLoS One 2011, 6:e27972.
13. Hayat M.A. Principles and Techniques of Electron Microscopy: Biological Applications 2000, Cambridge University Press. 4th edition.
14. Hoet P., Bruske-Hohlfeld I., Salata O.V. Nanoparticles - known and unknown health risks. J. Nanobiotechnol. 2004, 2:12.
15. Inoue K., Yanagisawa R., Koike E., Nishikawa M., Takano H. Repeated pulmonary exposure to single-walled carbon nanotubes exacerbates allergic inflammation of the airway: possible role of oxidative stress. Free Radic. Biol. Med. 2010, 48:924-934.
16. Janku F., McConkey D.J., Hong D.S., Kurzrock R. Autophagy as a target for anticancer therapy. Nat. Rev. Clin. Oncol. 2011, 8:528-539.
17. Jiang W., Kim B.Y., Rutka J.T., Warren C.W.C. Nanoparticle-mediated cellular response is size-dependent. Nat. Nanotechnol. 2008, 3:145-150.
18. Jiang J., Maeda A., Ji J., Baty C.J., Watkins S.C., Greenberger J.S., Kagan V.E. Are mitochondrial reactive oxygen species required for autophagy?. Biochem. Biophys. Res. Commun. 2011, 412:55-60.
19. Johnson-Lyles D.N., Peifley K., Lockett S., Neun B.W., Hansen M., Clogston J., Stern S.T., McNeil S.E. Fullerenol cytotoxicity in kidney cells is associated with cytoskeleton disruption, autophagic vacuole accumulation, and mitochondrial dysfunction. Toxicol. Appl. Pharmacol. 2010, 248:249-258.
20. Kabeya Y., Mizushima N., Ueno T., Yamamoto A., Kirisako T., Noda T., Kominami E., Ohsumi Y., Yoshimori T. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 2000, 19:5720-5728.
21. Kagan V.E., Bayir H., Shvedova A.A. Nanomedicine and nanotoxicology: two sides of the same coin. Nanomedicine 2005, 1:313-316.
22. Kagan V.E., Konduru N.V., Feng W., Allen B.L., Conroy J., Volkov Y., Vlasova I.I., Belikova N.A., Yanamala N., Kapralov A., Tyurina Y.Y., Shi J., Kisin E.R., Murray A.R., Franks J., Stolz D., Gou P., Klein-Seetharaman J., Fadeel B., Star A., Shvedova A.A. Carbon nanotubes degraded by neutrophil myeloperoxidase induce less pulmonary inflammation. Nat. Nanotechnol. 2010, 5:354-359.
23. Kaminskyy V., Abdi A., Zhivotovsky B. A quantitative assay for the monitoring of autophagosome accumulation in different phases of the cell cycle. Autophagy 2011, 7:83-90.
24. Karna P., Zughaier S., Pannu V., Simmons R., Narayan S., Aneja R. Induction of reactive oxygen species-mediated autophagy by a novel microtubule-modulating agent. J. Biol. Chem. 2010, 285:18737-18748.
25. Kenzaoui B.H., Bernasconi C.C., Guney-Ayra S., Juillerat-Jeanneret L. Induction of oxidative stress, lysosome activation and autophagy by nanoparticles in human brain-derived endothelial cells. Biochem. J. 2012, 441:813-821.
26. Kim S., Choi J.E., Choi J., Chung K.H., Park K., Yi J., Ryu D.Y. Oxidative stress-dependent toxicity of silver nanoparticles in human hepatoma cells. Toxicol. in Vitro 2009, 23:1076-1084.
27. Kirkegaard K., Taylor M.P., Jackson W.T. Cellular autophagy: surrender, avoidance and subversion by microorganisms. Nat. Rev. Microbiol. 2004, 2:301-314.
28. Klionsky D.J. Autophagy: from phenomenology to molecular understanding in less than a decade. Nat. Rev. Mol. Cell Biol. 2007, 8:931-937.
29. Kondo Y., Kanzawa T., Sawaya R., Kondo S. The role of autophagy in cancer development and response to therapy. Nat. Rev. Cancer 2005, 5:726-734.
30. Kroemer G., Levine B. Autophagic cell death: the story of a misnomer. Nat. Rev. Mol. Cell Biol. 2008, 9:1004-1010.
31. Kroemer G., Mariño G., Levine B. Autophagy and the integrated stress response. Mol. Cell 2010, 40:280-293.
32. Lee J.Y., Connor S.T., Cui Y., Peumans P. Solution-processed metal nanowire mesh transparent electrodes. Nano Lett. 2008, 8:689-692.
33. Lee M.S., Cherla R.P., Lentz E.K., Leyva-Illades D., Tesh V.L. Signaling through C/EBP homologous protein and death receptor 5 and calpain activation differentially regulate THP-1 cell maturation-dependent apoptosis induced by Shiga toxin type 1. Infect. Immun. 2010, 78:3378-3391.
34. Lee M.S., Cherla R.P., Jenson M.H., Leyva-Illades D., Martinez-Moczygemba M., Tesh V.L. Shiga toxins induce autophagy leading to differential signalling pathways in toxin-sensitive and toxin-resistant human cells. Cell. Microbiol. 2011, 13:1479-1496.
35. 60 fullerene-pentoxifylline dyad nanoparticles enhance autophagy to avoid cytotoxic effects caused by the β-amyloid peptide. Nanomedicine 2011, 7:107-114.
36. Lerena C., Calligaris S.D., Colombo M.I. Autophagy: for better or for worse, in good times or in bad times. Curr. Mol. Med. 2008, 8:92-101.
37. Li C., Liu H., Sun Y., Wang H., Guo F., Rao S., Deng J., Zhang Y., Miao Y., Guo C., Meng J., Chen X., Li L., Li D., Xu H., Wang H., Li B., Jiang C. PAMAM nanoparticles promote acute lung injury by inducing autophagic cell death through the Akt-TSC2-mTOR signaling pathway. J. Mol. Cell Biol. 2009, 1:37-45.
38. Li J.J., Hartono D., Ong C.N., Bay B.H., Yung L.Y. Autophagy and oxidative stress associated with gold nanoparticles. Biomaterials 2010, 31:5996-6003.
39. Liu C.H., Yu X. Silver nanowire-based transparent, flexible, and conductive thin film. Nanoscale Res. Lett. 2011, 6:75.
40. Liu H.L., Zhang Y.L., Yang N., Zhang Y.X., Liu X.Q., Li C.G., Zhao Y., Wang Y.G., Zhang G.G., Yang P., Guo F., Sun Y., Jiang C.Y. A functionalized single-walled carbon nanotubeinduced autophagic cell death in human lung cells through Akt-TSC2-mTOR signalling. Cell Death Dis. 2011, 2:e159.
41. Luft J.H. Improvements in epoxy embedding methods. J. Cell Biol. 1961, 9:409-414.
42. Luu Q.N., Doorn J.M., Berry M.T., Jiang C., Lin C., May P.S. Preparation and optical properties of silver nanowires and silver-nanowire thin films. J. Colloid Interface Sci. 2011, 356:151-158.
43. Maiuri M.C., Zalckvar E., Kimchi A., Kroemer G. Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat. Rev. Mol. Cell Biol. 2007, 8:741-752.
44. Martin T.R., Frevert C.W. Innate immunity in the lungs. Proc. Am. Thorac. Soc. 2005, 2:403-411.
45. Mathew R., Karantza-Wadsworth V., White E. Role of autophagy in cancer. Nat. Rev. Cancer 2007, 7:961-967.
46. Maynard A.D., Warheit D.B., Philbert M.A. The new toxicology of sophisticated materials: nanotoxicology and beyond. Toxicol. Sci. 2011, 120(Suppl. 1):S109-S129.
47. Mehrpour M., Esclatine A., Beau I., Codogno P. Autophagy in health and disease. 1. Regulation and significance of autophagy: an overview. Am. J. Physiol. Cell Physiol. 2010, 298:C776-C785.
48. 2 nanoparticles exposure as an early indicator of cytotoxicity. J. Nanobiotechnol. 2011, 9:29.
49. Mohamed B.M., Verma N.K., Davies A.M., McGowan A., Staunton K.C., Prina-Mello A., Kelleher D., Botting C.H., Causey C.P., Thompson P.R., Pruijn G.J.M., Kisin E.R., Tkach A.V., Shvedova A.A., Volkov Y. Citrullination of proteins: a common post-translational modification pathway induced by different nanoparticles in vitro and in vivo. Nanomedicine 2012, 7:1181-1195.
50. Moreau K., Luo S., Rubinsztein D.C. Cytoprotective roles for autophagy. Curr. Opin. Cell Biol. 2010, 22:206-211.
51. Moreira P.I., Santos R.X., Zhu X., Lee H.G., Smith M.A., Casadesus G., Perry G. Autophagy in Alzheimer's disease. Expert. Rev. Neurother. 2010, 10:1209-1218.
52. Moretti L., Cha Y.I., Niermann K.J., Lu B. Switch between apoptosis and autophagy: radiation-induced endoplasmic reticulum stress?. Cell Cycle 2007, 6:793-798.
53. Müller L., Riediker M., Wick P., Mohr M., Gehr P., Rothen-Rutishauser B. Oxidative stress and inflammation response after nanoparticle exposure: differences between human lung cell monocultures and an advanced three-dimensional model of the human epithelial airways. J. R. Soc. Interface 2010, 7:S27-S40.
54. Oberdorster G., Sharp Z., Atudorei V., Elder A., Gelein R., Lunts A., Kreyling W., Cox C. Extrapulmonary translocation of ultrafine carbon particles following whole-body inhalation exposure of rats. J. Toxicol. Environ. Health A 2002, 65:1531-1543.
55. Oberdorster G., Oberdorster E., Oberdorster J. Nanotoxicology: an emerging discipline evolving from studies of unltrafine particles. Environ. Health Perspect. 2005, 113:823-839.
56. Oberdörster G., Maynard A., Donaldson K., Castranova V., Fitzpatrick J., Ausman K., Carter J., Karn B., Kreyling W., Lai D., Olin S., Monteiro-Riviere N., Warheit D., Yang H. Principles for characterizing the potential human health effects from exposure to nanomaterials: elements of a screening strategy. Part Fibre Toxicol. 2005, 2:8. ILSI Research Foundation/Risk Science Institute Nanomaterial Toxicity Screening Working Group.
57. Ongondo F.O., Williams I.D., Cherrett T.J. How are WEEE doing? A global review of the management of electrical and electronic wastes. Waste Manag. 2011, 31:714-730.
58. Perlman Z.E., Slack M.D., Feng Y., Mitchison T.J., Wu L.F., Altschuler S.J. Multidimensional drug profiling by automated microscopy. Science 2004, 306:1194-1198.
59. Pluddemann A., Mukhopadhyay S., Gordon S. Innate immunity to intracellular pathogens: macrophage receptors and responses to microbial entry. Immunol. Rev. 2011, 240:11-24.
60. Rabinowitz J.D., White E. Autophagy and metabolism. Science 2010, 330:1344-1348.
61. Riendeau C.J., Kornfeld H. THP-1 cell apoptosis in response to mycobacterial infection. Infect. Immun. 2003, 71:254-259.
62. Santos-Martinez M.J., Medina C., Prina-Mello A., Conroy J., Samuels S.P., Volkov Y., Radomski M.W. A nanoscale resolution assay of flow-induced platelet microaggregation. Kardiochirurgia i Torakochirurgia Polska 2010, 7:365-375.
63. Scardaci V., Coull R., Lyons P.E., Rickard D., Coleman J.N. Spray deposition of highly transparent, low-resistance networks of silver nanowires over large areas. Small 2011, 7:2621-2628.
64. Scarlatti F., Maffei R., Beau I., Codogno P., Ghidoni R. Role of non-canonical Beclin 1-independent autophagy in cell death induced by resveratrol in human breast cancer cells. Cell Death Differ. 2008, 15:1318-1329.
65. Scarlatti F., Granata R., Meijer A.J., Codogno P. Does autophagy have a license to kill mammalian cells?. Cell Death Differ. 2009, 16:12-20.
66. Seleverstov O., Zabirnyk O., Zscharnack M., Bulavina L., Nowicki M., Heinrich J.M., Yezhelyev M., Emmrich F., O'Regan R., Bader A. Quantum dots for human mesenchymal stem cells labeling. A size-dependent autophagy activation. Nano Lett. 2006, 12:2826-2832.
67. Shvedova A.A., Pietroiusti A., Fadeel B., Kagan V.E. Mechanisms of carbon nanotube-induced toxicity: focus on oxidative stress. Toxicol. Appl. Pharmacol. 2012, 261:121-133.
68. Shvedova A.A., Kapralov A.A., Feng W.H., Kisin E.R., Murray A.R., Mercer R.R., St Croix C.M., Lang M.A., Watkins S.C., Konduru N.V., Allen B.L., Conroy J., Kotchey G.P., Mohamed B.M., Meade A.D., Volkov Y., Star A., Fadeel B., Kagan V.E. Impaired clearance and enhanced pulmonary inflammatory/fibrotic response to carbon nanotubes in myeloperoxidase-deficient mice. PLoS One 2012, 7:e30923.
69. Sibille Y., Reynolds H.Y. Macrophages and polymorphonuclear neutrophils in lung defense and injury. Am. Rev. Respir. Dis. 1990, 141:471-501.
70. Sorel S., Lyons P.E., De S., Dickerson J.C., Coleman J.N. The dependence of the optoelectrical properties of silver nanowire networks on nanowire length and diameter. Nanotechnology 2012, 23:1-9.
71. Stern S.T., Zolnik B.S., McLeland C.B., Clogston J., Zheng J., McNeil S.E. Induction of autophagy in porcine kidney cells by quantum dots: a common cellular response to nanomaterials?. Toxicol. Sci. 2008, 106:140-152.
72. Sun Y. Silver nanowires-unique templates for functional nanostructures. Nanoscale 2010, 2:1626-1642.
73. Tanida I., Ueno T., Kominami E. LC3 conjugation system in mammalian autophagy. Int. J. Biochem. Cell Biol. 2004, 36:2503-2518.
74. van de Groep J., Spinelli P., Polman A. Transparent conducting silver nanowire networks. Nano Lett. 2012, 12:3138-3144.
75. Vasir J.K., Labhasetwar V. Quantification of the force of nanoparticle-cell membrane interactions and its influence on intracellular trafficking of nanoparticles. Biomaterials 2008, 29:4244-4252.
76. Verma N.K., Dourlat J., Davies A.M., Long A., Liu W.Q., Garbay C., Kelleher D., Volkov Y. STAT3-stathmin interactions control microtubule dynamics in migrating T-cells. J. Biol. Chem. 2009, 284:12349-12362.
77. Verma N.K., Moore E., Blau W., Volkov Y., Babu R. Cytotoxicity evaluation of nanoclays in human epithelial cell line A549 using high content screening and real-time impedance analysis. J. Nanopart. Res. 2012, 14:1137.
78. Yuan H., Perry C.N., Huang C., Iwai-Kanai E., Carreira R.S., Glembotski C.C., Gottlieb R.A. LPS-induced autophagy is mediated by oxidative signaling in cardiomyocytes and is associated with cytoprotection. Am J Physiol Heart Circ Physiol 2009, 296:H470-H479.
79. Zabirnyk O., Yezhelyev M., Seleverstov O. Nanoparticles as a novel class of autophagy activators. Autophagy 2007, 3:278-281.
80. Zhang P., Summer W.R., Bagby G.J., Nelson S. Innate immunity and pulmonary host defence. Immunol. Rev. 2000, 173:39-51.
81. Zhu M.T., Feng W.Y., Wang Y., Wang B., Wang M., Ouyang H., Zhao Y.L., Chai Z.F. Particokinetics and extrapulmonary translocation of intratracheally instilled ferric oxide nanoparticles in rats and the potential health risk assessment. Toxicol. Sci. 2009, 107:342-351.
82. Zuin S., Micheletti C., Critto A., Pojana G., Johnston H., Stone V., Tran L., Marcomini A. Weight of evidence approach for the relative hazard ranking of nanomaterials. Nanotoxicology 2011, 5:445-458.