Molecular responses of alveolar epithelial A549 cells to chronic exposure to titanium dioxide nanoparticles: A proteomic view

Journal of Proteomics

Volumn 134, Issue , 2016, Pages 163-173

  Armand, Lucie ^a,b   Biola Clier, Mathilde ^a,b   Bobyk, Laure ^a,b   Collin Faure, Véronique ^b   Diemer, Hélène ^c,d   Strub, Jean Marc ^c,d   Cianferani, Sarah ^c,d   Van Dorsselaer, Alain ^c,d   Herlin Boime, Nathalie ^d   Rabilloud, Thierry ^e   Carriere, Marie ^a,b  

^a UNIV GRENOBLE ALPES   (France)

^b CEA GRENOBLE   (France)

^c UNIVERSITÉ DE STRASBOURG   (France)

^d CNRS   (France)

^e CEA SACLAY   (France)

Author keywords

A549; Chronic exposure; Long term exposure; Nanoparticle; Toxicity; Whole proteome expression

Indexed keywords

CHAPERONE; TITANIUM DIOXIDE NANOPARTICLE; NANOPARTICLE; PROTEOME; TITANIUM; TITANIUM DIOXIDE;

A549 CELL LINE; ARTICLE; CELL FUNCTION; CELL PROLIFERATION; CONTROLLED STUDY; DNA DAMAGE; GENE EXPRESSION; GLUCOSE METABOLISM; HOMEOSTASIS; HUMAN; HUMAN CELL; LONG TERM EXPOSURE; LUNG ALVEOLUS EPITHELIUM CELL; MITOCHONDRION; PRIORITY JOURNAL; PROTEIN TRANSPORT; PROTEOMICS; CHEMISTRY; EPITHELIUM CELL; LUNG ALVEOLUS; METABOLISM; RESPIRATORY MUCOSA; TUMOR CELL LINE;

CELL LINE, TUMOR; EPITHELIAL CELLS; HUMANS; NANOPARTICLES; PROTEOME; PROTEOMICS; PULMONARY ALVEOLI; RESPIRATORY MUCOSA; TITANIUM;

EID: 84958164156     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2015.08.006     Document Type: Article

References (67)

1. 2 production as a basis for exposure assessment. Environ. Sci. Technol. 2009, 43:4227-4233.
2. Oberdorster G., Oberdorster E., Oberdorster J. Nanotoxicology: an emerging discipline evolving from studies of ultrafine particles. Environ. Health Perspect. 2005, 113:823-839.
3. Loomis D., Grosse Y., Lauby-Secretan B., El Ghissassi F., Bouvard V., Benbrahim-Tallaa L., et al. The carcinogenicity of outdoor air pollution. Lancet Oncol. 2013, 14:1262-1263.
4. Shi H., Magaye R., Castranova V., Zhao J. Titanium dioxide nanoparticles: a review of current toxicological data. Part. Fibre Toxicol. 2013, 10.
5. Bernier M.C., Besse M., Vayssade M., Morandat S., El Kirat K. Titanium dioxide nanoparticles disturb the fibronectin-mediated adhesion and spreading of pre-osteoblastic cells. Langmuir 2012, 28:13660-13667.
6. Zarogiannis S.G., Filippidis A.S., Fernandez S., Jurkuvenaite A., Ambalavanan N., Stanishevsky A., et al. Nano-TiO(2) particles impair adhesion of airway epithelial cells to fibronectin. Respir. Physiol. Neurobiol. 2013, 185:454-460.
7. Zhao Y., Howe J.L., Yu Z., Leong D.T., Chu J.J., Loo J.S., et al. Exposure to titanium dioxide nanoparticles induces autophagy in primary human keratinocytes. Small 2013, 9:387-392.
8. Triboulet S., Aude-Garcia C., Armand L., Collin-Faure V., Chevallet M., Diemer H., et al. Comparative proteomic analysis of the molecular responses of mouse macrophages to titanium dioxide and copper oxide nanoparticles unravels some toxic mechanisms for copper oxide nanoparticles in macrophages. PLoS One 2015, 10:2015.
9. Ge Y., Bruno M., Wallace K., Winnik W., Prasad R.Y. Proteome profiling reveals potential toxicity and detoxification pathways following exposure of BEAS-2B cells to engineered nanoparticle titanium dioxide. Proteomics 2011, 11:2406-2422.
10. Gao Y., Gopee N.V., Howard P.C., Yu L.R. Proteomic analysis of early response lymph node proteins in mice treated with titanium dioxide nanoparticles. J. Proteomics 2011, 74:2745-2759.
11. Sund J., Palomaki J., Ahonen N., Savolainen K., Alenius H., Puustinen A. Phagocytosis of nano-sized titanium dioxide triggers changes in protein acetylation. J. Proteomics 2014, 108:469-483.
12. Tilton S.C., Karin N.J., Tolic A., Xie Y., Lai X., Hamilton R.F., et al. Three human cell types respond to multi-walled carbon nanotubes and titanium dioxide nanobelts with cell-specific transcriptomic and proteomic expression patterns. Nanotoxicology 2014, 8:533-548.
13. 2 long-term exposure. Toxicol. Appl. Pharmacol. 2009, 241:182-194.
14. 2 nanoparticles. Small 2010, 6:1908-1917.
15. Wang S., Hunter L.A., Arslan Z., Wilkerson M.G., Wickliffe J.K. Chronic exposure to nanosized, anatase titanium dioxide is not cyto- or genotoxic to Chinese hamster ovary cells. Environ. Mol. Mutagen. 2011, 52:614-622.
16. Vales G., Rubio L., Marcos R. Long-term exposures to low doses of titanium dioxide nanoparticles induce cell transformation, but not genotoxic damage in BEAS-2B cells. Nanotoxicology 2014, 19:1-11.
17. Human respiratory tract model for radiological protection. A report of a Task Group of the International Commission on Radiological Protection. Ann. ICRP 1994, 24:1-482.
18. Rabilloud T., Lescuyer P. Proteomics in mechanistic toxicology: history, concepts, achievements, caveats, and potential. Proteomics 2015, 15:1051-1074.
19. Simon-Deckers A., Gouget B., Mayne-L'Hermite M., Herlin-Boime N., Reynaud C., Carriere M. In vitro investigation of oxide nanoparticle and carbon nanotube toxicity and intracellular accumulation in A549 human pneumocytes. Toxicology 2008, 253:137-146.
20. Brun E., Barreau F., Veronesi G., Fayard B., Sorieul S., Chaneac C., et al. Titanium dioxide nanoparticle impact and translocation through ex vivo, in vivo and in vitro gut epithelia. Part. Fibre Toxicol. 2014, 11:1743-8977.
21. Jugan M.-L., Barillet S., Simon-Deckers A., Herlin-Boime N., Sauvaigo S., Douki T., et al. Titanium dioxide nanoparticles exhibit genotoxicity and impair DNA repair activity in A549 cells. Nanotoxicology 2012, 6:501-513.
22. Triboulet S., Aude-Garcia C., Armand L., Gerdil A., Diemer H., Proamer F., et al. Analysis of cellular responses of macrophages to zinc ions and zinc oxide nanoparticles: a combined targeted and proteomic approach. Nanoscale 2014, 6:6102-6114.
23. Gianazza E., Celentano F., Magenes S., Ettori C., Righetti P.G. Formulations for immobilized pH gradients including pH extremes. Electrophoresis 1989, 10:806-808.
24. Rabilloud T., Valette C., Lawrence J.J. Sample application by in-gel rehydration improves the resolution of two-dimensional electrophoresis with immobilized pH gradients in the first dimension. Electrophoresis 1994, 15:1552-1558.
25. Rabilloud T., Adessi C., Giraudel A., Lunardi J. Improvement of the solubilization of proteins in two-dimensional electrophoresis with immobilized pH gradients. Electrophoresis 1997, 18:307-316.
26. Luche S., Diemer H., Tastet C., Chevallet M., Van Dorsselaer A., Leize-Wagner E., et al. About thiol derivatization and resolution of basic proteins in two-dimensional electrophoresis. Proteomics 2004, 4:551-561.
27. Gorg A., Postel W., Gunther S., Weser J., Strahler J.R., Hanash S.M., et al. Approach to stationary two-dimensional pattern: influence of focusing time and immobiline/carrier ampholytes concentrations. Electrophoresis 1988, 9:37-46.
28. Tastet C., Lescuyer P., Diemer H., Luche S., van Dorsselaer A., Rabilloud T. A versatile electrophoresis system for the analysis of high- and low-molecular-weight proteins. Electrophoresis 2003, 24:1787-1794.
29. Chevallet M., Luche S., Rabilloud T. Silver staining of proteins in polyacrylamide gels. Nat. Protoc. 2006, 1:1852-1858.
30. Consortium U. UniProt: a hub for protein information. Nucleic Acids Res. 2015, 43:27.
31. Vizcaino J.A., Deutsch E.W., Wang R., Csordas A., Reisinger F., Rios D., et al. ProteomeXchange provides globally coordinated proteomics data submission and dissemination. Nat. Biotechnol. Mar 2014, 32(3):223-226. 10.1038/nbt.2839.
32. Pal-Bhowmick I., Sadagopan K., Vora H.K., Sehgal A., Sharma S., Jarori G.K. Cloning, over-expression, purification and characterization of Plasmodium falciparum enolase. Eur. J. Biochem. 2004, 271:4845-4854.
33. Unnithan A.S., Choi H.J., Titler A.M., Posimo J.M., Leak R.K. Rescue from a two hit, high-throughput model of neurodegeneration with N-acetyl cysteine. Neurochem. Int. 2012, 61:356-368.
34. Triboulet S., Aude-Garcia C., Carriere M., Diemer H., Proamer F., Habert A., et al. Molecular responses of mouse macrophages to copper and copper oxide nanoparticles inferred from proteomic analyses. Mol. Cell. Proteomics 2013, 12:3108-3122.
35. Dorier M., Brun E., Veronesi G., Barreau F., Pernet-Gallay K., Desvergne C., et al. Impact of anatase and rutile titanium dioxide nanoparticles on uptake carriers and efflux pumps in Caco-2 gut epithelial cells. Nanoscale 2015, 7:7352-7360.
36. Hoogland C., Mostaguir K., Sanchez J.C., Hochstrasser D.F., Appel R.D. SWISS-2DPAGE, ten years later. Proteomics 2004, 4:2352-2356.
37. Winkler D.F., McGeer P.L. Protein labeling and biotinylation of peptides during spot synthesis using biotin p-nitrophenyl ester (biotin-ONp). Proteomics 2008, 8:961-967.
38. Jehmlich N., Dinh K.H., Gesell-Salazar M., Hammer E., Steil L., Dhople V.M., et al. Quantitative analysis of the intra- and inter-subject variability of the whole salivary proteome. J. Periodontal Res. 2013, 48:392-403.
39. Wu J., Xie H. Effects of titanium dioxide nanoparticles on alpha-synuclein aggregation and the ubiquitin-proteasome system in dopaminergic neurons. Artif. Cells Nanomed. Biotechnol. 2014, 11:1-5.
40. Lee D.H., Goldberg A.L. Proteasome inhibitors: valuable new tools for cell biologists. Trends Cell Biol. 1998, 8:397-403.
41. Han Y.H., Park W.H. Proteasome inhibitor MG132 reduces growth of As4.1 juxtaglomerular cells via caspase-independent apoptosis. Arch. Toxicol. 2010, 84:689-698.
42. Yoshii S.R., Mizushima N. Autophagy machinery in the context of mammalian mitophagy. Biochim. Biophys. Acta Jan 26 2015, (pii: S0167-4889(15)00022-1). 10.1016/j.bbamcr.2015.01.013.
43. Demonacos C., Krstic-Demonacos M., Smith L., Xu D., O'Connor D.P., Jansson M., et al. A new effector pathway links ATM kinase with the DNA damage response. Nat. Cell Biol. 2004, 6:968-976.
44. Sakaguchi K., Herrera J.E., Saito S., Miki T., Bustin M., Vassilev A., et al. DNA damage activates p53 through a phosphorylation-acetylation cascade. Genes Dev. 1998, 12:2831-2841.
45. Macleod K.F., Sherry N., Hannon G., Beach D., Tokino T., Kinzler K., et al. p53-dependent and independent expression of p21 during cell growth, differentiation, and DNA damage. Genes Dev. 1995, 9:935-944.
46. Hinds T.D., Sanchez E.R. Protein phosphatase 5. Int. J. Biochem. Cell Biol. 2008, 40:2358-2362.
47. Ekstrand-Hammarstrom B., Akfur C.M., Andersson P.O., Lejon C., Osterlund L., Bucht A. Human primary bronchial epithelial cells respond differently to titanium dioxide nanoparticles than the lung epithelial cell lines A549 and BEAS-2B. Nanotoxicology 2012, 6:623-634.
48. 2 nanoparticles induce DNA double strand breaks and cell cycle arrest in human alveolar cells. Environ. Mol. Mutagen. 2015, 56:204-217.
49. Khan D., Katoch A., Das A., Sharathchandra A., Lal R., Roy P., et al. Reversible induction of translational isoforms of p53 in glucose deprivation. Cell Death Differ. 2015, 2015:220.
50. Speidel D. The role of DNA damage responses in p53 biology. Arch. Toxicol. 2015, 89:501-517.
51. Shiloh Y., Ziv Y. The ATM protein kinase: regulating the cellular response to genotoxic stress, and more. Nat. Rev. Mol. Cell Biol. 2013, 14:197-210.
52. Belade E., Chrusciel S., Armand L., Simon-Deckers A., Bussy C., Caramelle P., et al. The role of p53 in lung macrophages following exposure to a panel of manufactured nanomaterials. Arch. Toxicol. 2014, 2014:7.
53. Marquez-Ramirez S.G., Delgado-Buenrostro N.L., Chirino Y.I., Iglesias G.G., Lopez-Marure R. Titanium dioxide nanoparticles inhibit proliferation and induce morphological changes and apoptosis in glial cells. Toxicology 2012, 302:146-156.
54. Prasad R.Y., Chastain P.D., Nikolaishvili-Feinberg N., Smeester L., Kaufmann W.K., Fry R.C. Titanium dioxide nanoparticles activate the ATM-Chk2 DNA damage response in human dermal fibroblasts. Nanotoxicology 2013, 7:1111-1119.
55. Montague C.R., Fitzmaurice A., Hover B.M., Salazar N.A., Fey J.P. Screen for small molecules increasing the mitochondrial membrane potential. J. Biomol. Screen. 2014, 19:387-398.
56. Paglin S., Lee N.Y., Nakar C., Fitzgerald M., Plotkin J., Deuel B., et al. Rapamycin-sensitive pathway regulates mitochondrial membrane potential, autophagy, and survival in irradiated MCF-7 cells. Cancer Res. 2005, 65:11061-11070.
57. Jangamreddy J.R., Ghavami S., Grabarek J., Kratz G., Wiechec E., Fredriksson B.A., et al. Salinomycin induces activation of autophagy, mitophagy and affects mitochondrial polarity: differences between primary and cancer cells. Biochim. Biophys. Acta 2013, 2013:2057-2069.
58. Kumari S., Mehta S.L., Li P.A. Glutamate induces mitochondrial dynamic imbalance and autophagy activation: preventive effects of selenium. PLoS One 2012, 7:19.
59. Stern S.T., Adiseshaiah P.P., Crist R.M. Autophagy and lysosomal dysfunction as emerging mechanisms of nanomaterial toxicity. Part. Fibre Toxicol. 2012, 9:1743-8977.
60. Tang Y., Wang F., Jin C., Liang H., Zhong X., Yang Y. Mitochondrial injury induced by nanosized titanium dioxide in A549 cells and rats. Environ. Toxicol. Pharmacol. 2013, 36:66-72.
61. Kalmar B., Greensmith L. Induction of heat shock proteins for protection against oxidative stress. Adv. Drug Deliv. Rev. 2009, 61:310-318.
62. Esser C., Alberti S., Hohfeld J. Cooperation of molecular chaperones with the ubiquitin/proteasome system. Biochim. Biophys. Acta 2004, 29:1-3.
63. Wu K.C., Jin J.P. Calponin in non-muscle cells. Cell Biochem. Biophys. 2008, 52:139-148.
64. Willshaw A., Grant K., Yan J., Rockliffe N., Ambavarapu S., Burdyga G., et al. Identification of a novel protein complex containing annexin A4, rabphilin and synaptotagmin. FEBS Lett. 2004, 559:13-21.
65. Keating D.J. Mitochondrial dysfunction, oxidative stress, regulation of exocytosis and their relevance to neurodegenerative diseases. J. Neurochem. 2008, 104:298-305.
66. Vaughan P.S., Leszyk J.D., Vaughan K.T. Cytoplasmic dynein intermediate chain phosphorylation regulates binding to dynactin. J. Biol. Chem. 2001, 276:26171-26179.
67. Hirokawa N., Noda Y., Tanaka Y., Niwa S. Kinesin superfamily motor proteins and intracellular transport. Nat. Rev. Mol. Cell Biol. 2009, 10:682-696.