Titanium dioxide nanoparticles induce endoplasmic reticulum stress-mediated autophagic cell death via mitochondria-associated endoplasmic reticulum membrane disruption in normal lung cells

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Yu, Kyeong Nam ^a   Chang, Seung Hee ^a   Park, Soo Jin ^b   Lim, Joohyun ^a   Lee, Jinkyu ^a   Yoon, Tae Jong ^c   Kim, Jun Sung ^b   Cho, Myung Haing ^a,d  

^a Seoul National University   (South Korea)

^b R AndD Center Biterials Co   (South Korea)

^c CHA University   (South Korea)

^d Seoul National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM ION; CALNEXIN; CYTOCHROME C; CYTOCHROME C OXIDASE; CYTOCHROME C OXIDASE IV; GLUCOSE REGULATED PROTEIN 78; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; INOSITOL TRIPHOSPHATE RECEPTOR; PROTEIN IRE1; PROTEIN IRE1ALPHA; REACTIVE OXYGEN METABOLITE; RECEPTOR; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SUCCINATE DEHYDROGENASE (UBIQUINONE); TAUROURSODEOXYCHOLIC ACID; TITANIUM DIOXIDE NANOPARTICLE; UNCLASSIFIED DRUG; VOLTAGE DEPENDENT ANION CHANNEL 1; CALCIUM; NANOPARTICLE; TAUROCHENODEOXYCHOLIC ACID; TITANIUM; TITANIUM DIOXIDE;

ARTICLE; AUTOPHAGIC CELL DEATH; CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; CALCIUM TRANSPORT; CELL DEATH; CELL PROLIFERATION; CELL VIABILITY; CELLULAR DISTRIBUTION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOTOXICITY; CYTOTOXICITY TEST; ENDOPLASMIC RETICULUM STRESS; HUMAN; HUMAN CELL; INCUBATION TIME; LUNG ALVEOLUS CELL; MEMBRANE DAMAGE; MITOCHONDRIA ASSOCIATED ENDOPLASMIC RETICULUM MEMBRANE; MITOCHONDRIAL MEMBRANE; MOLECULAR DYNAMICS; MOLECULAR STABILITY; PARTICLE SIZE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; STRUCTURE ANALYSIS; SURFACE CHARGE; ZETA POTENTIAL; AUTOPHAGY; CELL CULTURE; DRUG EFFECTS; ENDOPLASMIC RETICULUM; EPITHELIUM CELL; HOMEOSTASIS; INTRACELLULAR MEMBRANE; LUNG; METABOLISM; MITOCHONDRION; PATHOLOGY; ULTRASTRUCTURE;

AUTOPHAGY; CALCIUM; CELLS, CULTURED; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; EPITHELIAL CELLS; HOMEOSTASIS; HUMANS; INTRACELLULAR MEMBRANES; LUNG; MITOCHONDRIA; NANOPARTICLES; REACTIVE OXYGEN SPECIES; TAUROCHENODEOXYCHOLIC ACID; TITANIUM;

EID: 84938629238     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0131208     Document Type: Article

References (47)

1. Afaq F, Abidi P, Matin R., Rahman Q. Cytotoxicity, pro-oxidant effects and antioxidant depletion in rat lung alveolar macrophages exposed to ultrafine titanium dioxide. J Appl Toxicol. 1998; 18: 307-312. PMID: 9804429
2. Gwinn MR, Vallyathan V. Nanoparticles: Health effects-pros and cons. Environ Health Perspect. 2006; 114: 1818-1825. PMID: 17185269
3. Long TC, Tajuba J, Sama P, Saleh N, Swartz C, Parker J, et al. Nanosize titanium dioxide stimulates reactive oxygen species in brain microglia and damages neurons in vitro. Environ Health Perspect. 2007; 115: 1631-1637. PMID: 18007996
4. Shi H, Magaye R, Castranova V, Zhao J. Titanium dioxide nanoparticles: a review of current toxicological data. Part Fibre Toxicol. 2013; 10: 15. doi: 10.1186/1743-8977-10-15 PMID: 23587290
5. Yin ZF, Wu L, Yang HG, Su YH. Recent progress in biomedical applications of titanium dioxide. Phys Chem Chem Phys. 2013; 15: 4844-4858. doi: 10.1039/c3cp43938k PMID: 23450160
6. Li J, Wang X, Jiang H, Lu X, Zhu Y, Chen B. New strategy of photodynamic treatment of TiO2 nanofibers combined with celastrol for HepG2 proliferation in vitro. Nanoscale. 2011; 3: 3115-3122. doi: 10. 1039/c1nr10185d PMID: 21666907
7. Triesscheijn M, Baas P, Schellens JH, Stewart FA. Photodynamic therapy in oncology. Oncologist. 2006; 11: 1034-1044. PMID: 17030646
8. Bhattacharya K, Davoren M, Boertz J, Schins RP, Hoffmann E, Dopp E. Titanium dioxide nanoparticles induce oxidative stress and DNA-adduct formation but not DNA-breakage in human lung cells. Part. Fibre Toxicol. 2009; 6: 17. doi: 10.1186/1743-8977-6-17 PMID: 19545397
9. 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.
10. Oesch F, Landsiedel R. Genotoxicity investigations on nanomaterials. Arch. Toxicol. 2012; 86: 985-994. doi: 10.1007/s00204-012-0838-y PMID: 22456836
11. Sager TM, Kommineni C, Castranova V. Pulmonary response to intratracheal instillation of ultrafine versus fine titanium dioxide: role of particle surface area. Part Fibre Toxicol 2008; 5:17. doi: 10.1186/1743-8977-5-17 PMID: 19046442
12. Oberdorster G, Ferin J, Lehnert BE. Correlation between particle size, in vivo particle persistence, and lung injury. Environ Health Perspect. 1994; 102:173-179.
13. Ferin J, Oberdörster G, Penney DP. Pulmonary retention of ultrafine and fine particles in rats. Am. J. Respir. Cell Mol. Biol. 1992; 6: 535-542. PMID: 1581076
14. Malhotra JD, Kaufman RJ. ER stress and its functional link to mitochondria: role in cell survival and death. Cold Spring Harb Perspect Biol. 2011; 3: a004424. doi: 10.1101/cshperspect.a004424 PMID: 21813400
15. van Vliet AR, Verfaillie T, Agostinis P. New functions of mitochondria associated membranes in cellular signaling. Biochim Biophys Acta. 2014; 1843: 2253-2262. doi: 10.1016/j.bbamcr.2014.03.009 PMID: 24642268
16. Bernales S, McDonald KL, Walter P. Autophagy counterbalances endoplasmic reticulum expansion during the unfolded protein response. PLoS Biol. 2006; 4: e423. PMID: 17132049
17. Yu KN, Yoon TJ, Minai-Tehrani A, Kim JE, Park SJ, Jeong MS, et al. Zinc oxide nanoparticle induced autophagic cell death and mitochondrial damage via reactive oxygen species generation. Toxicol In Vitro. 2013; 27: 1187-1195. doi: 10.1016/j.tiv.2013.02.010 PMID: 23458966
18. Jeong MS, Cho HS, Park SJ, Song KS, Ahn KS, Cho MH, et al. Physico-chemical characterization-based safety evaluation of nanocalcium. Food Chem Toxicol. 2013; 62: 308-317. doi: 10.1016/j.fct.2013.08.024 PMID: 23959102
19. Murdock RC, Braydich-Stolle L, Schrand AM, Schlager JJ, Hussain SM. Characterization of nanomaterial dispersion in solution prior to in vitro exposure using dynamic light scattering technique Toxicol Sci. 2008; 101:239-253. PMID: 17872897
20. Kahn BB, Alquier T, Carling D, Hardie DG. AMP-activated protein kinase: ancient energy gauge provides clues to modern understanding of metabolism. Cell Metab. 2005; 1: 15-25. PMID: 16054041
21. Meyer T, Wensel T, Stryer L. Kinetics of calcium channel opening by inositol 1,4,5-trisphosphate. Biochemistry. 1990; 29: 32-37. PMID: 1691015
22. Lihavainen E, Mäkelä J, Spelbrink JN, Ribeiro AS. Mytoe: automatic analysis of mitochondrial dynamics. Bioinformatics. 2012; 28: 1050-1051. doi: 10.1093/bioinformatics/bts073 PMID: 22321700
23. Shim SE, Lee H, Choe S. Synthesis of Functionalized Monodisperse Poly(methyl methacrylate) Nanoparticles by a RAFT Agent Carrying Carboxyl End Group. Macromolecules. 2004; 37: 5565-5571.
24. Papa FR, Zhang C, Shokat K, Walter P. Bypassing a kinase activity with an ATP-competitive drug. Science. 2003; 302: 1533-1537. PMID: 14564015
25. Schrag JD, Bergeron JJ, Li Y, Borisova S, Hahn M, Thomas DY, et al. The Structure of calnexin, an ER chaperone involved in quality control of protein folding. Mol Cell. 2001; 8: 633-644. PMID: 11583625
26. Torres M, Encina G, Soto C, Hetz C. Abnormal calcium homeostasis and protein folding stress at the ER: A common factor in familial and infectious prion disorders. Commun Integr Biol. 2011; 4: 258-261. doi: 10.4161/cib.4.3.15019 PMID: 21980554
27. González-Rodríguez A, Mayoral R, Agra N, Valdecantos MP, Pardo V, Miquilena-Colina ME, et al. Impaired autophagic flux is associated with increased endoplasmic reticulum stress during the development of NAFLD. Cell Death Dis. 2014; 17: e1179.
28. Kadowaki M, Karim MR. Cytosolic LC3 ratio as a quantitative index of macroautophagy. Methods Enzymol. 2009; 452: 199-213. doi: 10.1016/S0076-6879(08)03613-6 PMID: 19200884
29. Miller SD, Greene CM, McLean C, Lawless MW, Taggart CC., O'Neill SJ, et al. Tauroursodeoxycholic acid inhibits apoptosis induced by Z alpha-1 antitrypsin via inhibition of Bad. Hepatology. 2007; 46: 496-503. PMID: 17559149
30. Apopa PL, Qian Y, Shao R, Guo NL, Schwegler-Berry D, Pacurari M, et al. Iron oxide NPs induce human microvascular endothelial cell permeability through reactive oxygen species production and microtubule remodeling. Part Fibre Toxicol. 2009; 6: 1-14. doi: 10.1186/1743-8977-6-1 PMID: 19134195
31. Naqvi S, Samim M, Abdin M, Ahmed FJ, Maitra A, Prashant C, et al. Concentration-dependent toxicity of iron oxide nanoparticles mediated by increased oxidative stress. Int J Nanomedicine. 2010; 5: 983-989. doi: 10.2147/IJN.S13244 PMID: 21187917
32. Buyukhatipoglu K, Clyne AM. Superparamagnetic iron oxide nanoparticles change endothelial cell morphology and mechanics via reactive oxygen species formation. J Biomed Mater Res A. 2011; 96: 187-195.
33. Nel A, Xia T, Madler L, Li N. Toxic potential of materials at the nanolevel. Science. 2006; 311: 622-627. PMID: 16456071
34. Du H, Zhu X, Fan C, Xu S, Wang Y, Zhou Y. Oxidative damage and OGG1 expression induced by a combined effect of titanium dioxide nanoparticles and lead acetate in human hepatocytes. Environ Toxicol. 2012; 27:590-597. doi: 10.1002/tox.20682 PMID: 21254323
35. Saquib Q, Al-Khedhairy AA, Siddiqui MA, Abou-Tarboush FM, Azam A, Musarrat J. Titanium dioxide nanoparticles induced cytotoxicity, oxidative stress and DNA damage in human amnion epithelial (WISH) cells. Toxicol In Vitro. 2012; 26:351-361. doi: 10.1016/j.tiv.2011.12.011 PMID: 22210200
36. Groenendyk J, Sreenivasaiah PK, Kim do H, Agellon L B, Michalak M. Biology of endoplasmic reticulum stress in the heart. Circ Res. 2010; 107:1185-1197. doi: 10.1161/CIRCRESAHA.110.227033 PMID: 21071716
37. Kozutsumi Y, Segal M, Normington K, Gething MJ, Sambrook J. The presence of malfolded proteins in the endoplasmic reticulum signals the induction of glucose-regulated proteins. Nature. 1988; 332:462-464. PMID: 3352747
38. Christopher CG. Endoplasmic reticulum stress in the heart. Circ Res. 2007; 101: 975-984. PMID: 17991891
39. Yang X, Shao H, Liu W, Gu W, Shu X, Mo Y, Chen X, Zhang Q, Jiang M. Endoplasmic reticulum stress and oxidative stress are involved in ZnO nanoparticle-induced hepatotoxicity. Toxicol Lett. 2015; 234:40-49. doi: 10.1016/j.toxlet.2015.02.004 PMID: 25680694
40. Simard JC, Vallieres F, de Liz R, Lavastre V, Girard D. Silver nanoparticles induce degradation of the endoplasmic reticulum stress sensor activating transcription factor-6 leading to activation of the NLRP- 3 inflammasome. J Biol Chem. 2015; 290:5926-5939. doi: 10.1074/jbc.M114.610899 PMID: 25593314
41. Park EJ, Choi DH, Kim Y, Lee EW, Song J, Cho MH, Kim JH, Kim SW. Magnetic iron oxide nanoparticles induce autophagy preceding apoptosis through mitochondrial damage and ER stress in RAW264.7 cells. Toxicol In Vitro. 2014; 28:1402-1412. doi: 10.1016/j.tiv.2014.07.010 PMID: 25086211
42. Pozzan T, Rizzuto R. High tide of calcium in mitochondria. Nat Cell Biol. 2000; 2: 25-27. PMID: 10620803
43. Bernardi P, Petronilli V, Di Lisa F, Forte M. A mitochondrial perspective on cell death. Trends Biochem Sci. 2001; 26: 112-117. PMID: 11166569
44. Rizzuto R, Pinton P, Carrington W, Fay FS, Fogarty KE, Lifshitz LM, et al. Close contacts with the endoplasmic reticulum as determinants of mitochondrial Ca2+ responses. Science. 1998; 280: 1763-1766. PMID: 9624056
45. Szabadkai G, Bianchi K, Várnai P, De Stefani D, Wieckowski MR, Cavagna D, et al. Chaperone-mediated coupling of endoplasmic reticulum and mitochondrial Ca2+ channels. J Cell Biol. 2006; 175: 901-911. PMID: 17178908
46. Sano R, Hou YC, Hedvat M, Correa RG, Shu CW, Krajewska M, et al. Endoplasmic reticulum protein BI-1 regulates Ca2+-mediated bioenergetics to promote autophagy. Genes Dev. 2012; 26: 1041-1054. doi: 10.1101/gad.184325.111 PMID: 22588718
47. Decuypere JP, Welkenhuyzen K, Luyten T, Ponsaerts R, Dewaele M, Molgó J, et al. Ins(1,4,5)P3 receptor-mediated Ca2+ signaling and autophagy induction are interrelated. Autophagy 2011; 7: 1472-1489. PMID: 22082873