Carbon black and titanium dioxide nanoparticles elicit distinct apoptotic pathways in bronchial epithelial cells

Warheit DB, Sayes CM, Reed KL, Swain KA: Health effects related to nanoparticle exposures: environmental, health and safety considerations for assessing hazards and risks. Pharmacol Ther 2008, 120: 35–42. 10.1016/j.pharmthera.2008.07.001

Frampton MW, Utell MJ, Zareba W, Oberdorster G, Cox C, Huang LS, Morrow PE, Lee FE, Chalupa D, Frasier LM, Speers DM, Stewart J: Effects of exposure to ultrafine carbon particles in healthy subjects and subjects with asthma. Res Rep Health Eff Inst 2004, 1–47.

Oberdorster G: Pulmonary effects of inhaled ultrafine particles. Int Arch Occup Environ Health 2001, 74: 1–8. 10.1007/s004200000185

Nemmar A, Vanbilloen H, Hoylaerts MF, Hoet PH, Verbruggen A, Nemery B: Passage of intratracheally instilled ultrafine particles from the lung into the systemic circulation in hamster. Am J Respir Crit Care Med 2001, 164: 1665–1668.

Simeonova PP, Erdely A: Engineered nanoparticle respiratory exposure and potential risks for cardiovascular toxicity: predictive tests and biomarkers. Inhal Toxicol 2009, 21(Suppl 1):68–73. 10.1080/08958370902942566

Onuma K, Sato Y, Ogawara S, Shirasawa N, Kobayashi M, Yoshitake J, Yoshimura T, Iigo M, Fujii J, Okada F: Nano-Scaled Particles of Titanium Dioxide Convert Benign Mouse Fibrosarcoma Cells into Aggressive Tumor Cells. Am J Pathol 2009.

Long TC, Saleh N, Tilton RD, Lowry GV, Veronesi B: Titanium dioxide (P25) produces reactive oxygen species in immortalized brain microglia (BV2): implications for nanoparticle neurotoxicity. Environ Sci Technol 2006, 40: 4346–4352. 10.1021/es060589n

Xia T, Kovochich M, Nel A: The role of reactive oxygen species and oxidative stress in mediating particulate matter injury. Clin Occup Environ Med 2006, 5: 817–836.

Mueller NC, Nowack B: Exposure modeling of engineered nanoparticles in the environment. Environ Sci Technol 2008, 42: 4447–4453. 10.1021/es7029637

Robichaud CO, Uyar AE, Darby MR, Zucker LG, Wiesner MR: Estimates of upper bounds and trends in nano-TiO2 production as a basis for exposure assessment. Environ Sci Technol 2009, 43: 4227–4233. 10.1021/es8032549

Nel A, Xia T, Madler L, Li N: Toxic potential of materials at the nanolevel. Science 2006, 311: 622–627. 10.1126/science.1114397

Shi Y: Mechanisms of caspase activation and inhibition during apoptosis. Mol Cell 2002, 9: 459–470. 10.1016/S1097-2765(02)00482-3

Kasahara Y, Tuder RM, Taraseviciene-Stewart L, Le Cras TD, Abman S, Hirth PK, Waltenberger J, Voelkel NF: Inhibition of VEGF receptors causes lung cell apoptosis and emphysema. J Clin Invest 2000, 106: 1311–1319. 10.1172/JCI10259

Melis M, Siena L, Pace E, Gjomarkaj M, Profita M, Pirazzoli A, Todaro M, Stassi G, Bonsignore G, Vignola AM: Fluticasone induces apoptosis in peripheral T-lymphocytes: a comparison between asthmatic and normal subjects. Eur Respir J 2002, 19: 257–266. 10.1183/09031936.02.00239202

Suzuki YJ, Forman HJ, Sevanian A: Oxidants as stimulators of signal transduction. Free Radic Biol Med 1997, 22: 269–285. 10.1016/S0891-5849(96)00275-4

Kannan K, Jain SK: Oxidative stress and apoptosis. Pathophysiology 2000, 7: 153–163. 10.1016/S0928-4680(00)00053-5

Zamzami N, Marchetti P, Castedo M, Decaudin D, Macho A, Hirsch T, Susin SA, Petit PX, Mignotte B, Kroemer G: Sequential reduction of mitochondrial transmembrane potential and generation of reactive oxygen species in early programmed cell death. J Exp Med 1995, 182: 367–377. 10.1084/jem.182.2.367

Baumgartner HK, Gerasimenko JV, Thorne C, Ashurst LH, Barrow SL, Chvanov MA, Gillies S, Criddle DN, Tepikin AV, Petersen OH, Sutton R, Watson AJ, Gerasimenko OV: Caspase-8-mediated apoptosis induced by oxidative stress is independent of the intrinsic pathway and dependent on cathepsins. Am J Physiol Gastrointest Liver Physiol 2007, 293: G296-G307. 10.1152/ajpgi.00103.2007

Gurr JR, Wang AS, Chen CH, Jan KY: Ultrafine titanium dioxide particles in the absence of photoactivation can induce oxidative damage to human bronchial epithelial cells. Toxicology 2005, 213: 66–73. 10.1016/j.tox.2005.05.007

Limbach LK, Wick P, Manser P, Grass RN, Bruinink A, Stark WJ: Exposure of engineered nanoparticles to human lung epithelial cells: influence of chemical composition and catalytic activity on oxidative stress. Environ Sci Technol 2007, 41: 4158–4163. 10.1021/es062629t

Hussain S, Boland S, Baeza-Squiban A, Hamel R, Thomassen LC, Martens JA, Billon-Galland MA, Fleury-Feith J, Moisan F, Pairon JC, Marano F: Oxidative stress and proinflammatory effects of carbon black and titanium dioxide nanoparticles: role of particle surface area and internalized amount. Toxicology 2009, 260: 142–149. 10.1016/j.tox.2009.04.001

Sydlik U, Bierhals K, Soufi M, Abel J, Schins RP, Unfried K: Ultrafine carbon particles induce apoptosis and proliferation in rat lung epithelial cells via specific signaling pathways both using EGF-R. Am J Physiol Lung Cell Mol Physiol 2006, 291: L725-L733. 10.1152/ajplung.00131.2006

Pan Y, Neuss S, Leifert A, Fischler M, Wen F, Simon U, Schmid G, Brandau W, Jahnen-Dechent W: Size-dependent cytotoxicity of gold nanoparticles. Small 2007, 3: 1941–1949. 10.1002/smll.200700378

Pan Y, Leifert A, Ruau D, Neuss S, Bornemann J, Schmid G, Brandau W, Simon U, Jahnen-Dechent W: Gold nanoparticles of diameter 1.4 nm trigger necrosis by oxidative stress and mitochondrial damage. Small 2009, 5: 2067–2076. 10.1002/smll.200900466

Li N, Hao M, Phalen RF, Hinds WC, Nel AE: Particulate air pollutants and asthma. A paradigm for the role of oxidative stress in PM-induced adverse health effects. Clin Immunol 2003, 109: 250–265. 10.1016/j.clim.2003.08.006

Phalen RF, Oldham MJ, Nel AE: Tracheobronchial particle dose considerations for in vitro toxicology studies. Toxicol Sci 2006, 92: 126–132. 10.1093/toxsci/kfj182

Thomassen LC, Aerts A, Rabolli V, Lison D, Gonzalez L, Kirsch-Volders M, Napierska D, Hoet PH, Kirschhock CE, Martens JA: Synthesis and characterization of stable monodisperse silica nanoparticle sols for in vitro cytotoxicity testing. Langmuir 2010, 26: 328–335. 10.1021/la902050k

Brinker CJ, Scherer GW: Sol-Gel Science: The Physics and Chemistry of Sol-Gel Processing. 2nd edition. London: Academic Press; 1990.

Soto K, Garza KM, Murr LE: Cytotoxic effects of aggregated nanomaterials. Acta Biomater 2007, 3: 351–358. 10.1016/j.actbio.2006.11.004

Kerr JF, Wyllie AH, Currie AR: Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 1972, 26: 239–257.

Song Y, Li X, Du X: Exposure to nanoparticles is related to pleural effusion, pulmonary fibrosis and granuloma. Eur Respir J 2009, 34: 559–567. 10.1183/09031936.00178308

Bortner CD, Cidlowski JA: Apoptotic volume decrease and the incredible shrinking cell. Cell Death Differ 2002, 9: 1307–1310. 10.1038/sj.cdd.4401126

Park EJ, Choi J, Park YK, Park K: Oxidative stress induced by cerium oxide nanoparticles in cultured BEAS-2B cells. Toxicology 2008, 245: 90–100. 10.1016/j.tox.2007.12.022

Niazi S, Robertson NM, Agrawal A, Hastie AT, Peters SP, Zangrilli J: Overlap between death receptor and non-receptor-mediated mechanisms during apoptosis in human eosinophils. Chest 2003, 123: 345S. 10.1378/chest.123.3_suppl.345S

Sohn D, Schulze-Osthoff K, Janicke RU: Caspase-8 can be activated by interchain proteolysis without receptor-triggered dimerization during drug-induced apoptosis. J Biol Chem 2005, 280: 5267–5273. 10.1074/jbc.M408585200

Izeradjene K, Douglas L, Tillman DM, Delaney AB, Houghton JA: Reactive oxygen species regulate caspase activation in tumor necrosis factor-related apoptosis-inducing ligand-resistant human colon carcinoma cell lines. Cancer Res 2005, 65: 7436–7445. 10.1158/0008-5472.CAN-04-2628

Thornberry NA, Lazebnik Y: Caspases: enemies within. Science 1998, 281: 1312–1316. 10.1126/science.281.5381.1312

Hampton MB, Orrenius S: Redox regulation of apoptotic cell death in the immune system. Toxicol Lett 1998, 102–103: 355–358. 10.1016/S0378-4274(98)00333-6

Beckman JS, Minor RL Jr, Freeman BA: Augmentation of antioxidant enzymes in vascular endothelium. J Free Radic Biol Med 1986, 2: 359–365. 10.1016/S0748-5514(86)80036-8

Boya P, Kroemer G: Lysosomal membrane permeabilization in cell death. Oncogene 2008, 27: 6434–6451. 10.1038/onc.2008.310

Taylor RC, Cullen SP, Martin SJ: Apoptosis: controlled demolition at the cellular level. Nat Rev Mol Cell Biol 2008, 9: 231–241. 10.1038/nrm2312

Youle RJ, Strasser A: The BCL-2 protein family: opposing activities that mediate cell death. Nat Rev Mol Cell Biol 2008, 9: 47–59. 10.1038/nrm2308

Broker LE, Kruyt FA, Giaccone G: Cell death independent of caspases: a review. Clin Cancer Res 2005, 11: 3155–3162. 10.1158/1078-0432.CCR-04-2223

Broker LE, Huisman C, Span SW, Rodriguez JA, Kruyt FA, Giaccone G: Cathepsin B mediates caspase-independent cell death induced by microtubule stabilizing agents in non-small cell lung cancer cells. Cancer Res 2004, 64: 27–30. 10.1158/0008-5472.CAN-03-3060

Guicciardi ME, Leist M, Gores GJ: Lysosomes in cell death. Oncogene 2004, 23: 2881–2890. 10.1038/sj.onc.1207512

Leist M, Jaattela M: Triggering of apoptosis by cathepsins. Cell Death Differ 2001, 8: 324–326. 10.1038/sj.cdd.4400859

Zhao M, Eaton JW, Brunk UT: Bcl-2 phosphorylation is required for inhibition of oxidative stress-induced lysosomal leak and ensuing apoptosis. FEBS Lett 2001, 509: 405–412. 10.1016/S0014-5793(01)03185-4

Boya P, Andreau K, Poncet D, Zamzami N, Perfettini JL, Metivier D, Ojcius DM, Jaattela M, Kroemer G: Lysosomal membrane permeabilization induces cell death in a mitochondrion-dependent fashion. J Exp Med 2003, 197: 1323–1334. 10.1084/jem.20021952

Guicciardi ME, Deussing J, Miyoshi H, Bronk SF, Svingen PA, Peters C, Kaufmann SH, Gores GJ: Cathepsin B contributes to TNF-alpha-mediated hepatocyte apoptosis by promoting mitochondrial release of cytochrome c. J Clin Invest 2000, 106: 1127–1137. 10.1172/JCI9914

Thibodeau MS, Giardina C, Knecht DA, Helble J, Hubbard AK: Silica-induced apoptosis in mouse alveolar macrophages is initiated by lysosomal enzyme activity. Toxicol Sci 2004, 80: 34–48. 10.1093/toxsci/kfh121

Dare E, Li W, Zhivotovsky B, Yuan X, Ceccatelli S: Methylmercury and H(2)O(2) provoke lysosomal damage in human astrocytoma D384 cells followed by apoptosis. Free Radic Biol Med 2001, 30: 1347–1356. 10.1016/S0891-5849(01)00526-3

Terman A, Kurz T, Gustafsson B, Brunk UT: Lysosomal labilization. IUBMB Life 2006, 58: 531–539. 10.1080/15216540600904885

Fenoglio I, Greco G, Livraghi S, Fubini B: Non-UV-induced radical reactions at the surface of TiO2 nanoparticles that may trigger toxic responses. Chemistry 2009, 15: 4614–4621. 10.1002/chem.200802542

Liu W, Kato M, Akhand AA, Hayakawa A, Suzuki H, Miyata T, Kurokawa K, Hotta Y, Ishikawa N, Nakashima I: 4-hydroxynonenal induces a cellular redox status-related activation of the caspase cascade for apoptotic cell death. J Cell Sci 2000, 113: 635–641.

L'azou B, Jorly J, On D, Sellier E, Moisan F, Fleury-Feith J, Cambar J, Brochard P, Ohayon-Court : In vitro effects of nanoparticles on renal cells. Part Fibre Toxicol 2008, 5: 22. 10.1186/1743-8977-5-22

Setyan A, Sauvain JJ, Rossi MJ: The use of heterogeneous chemistry for the characterization of functional groups at the gas/particle interface of soot and TiO2 nanoparticles. Phys Chem Chem Phys 2009, 11: 6205–6217. 10.1039/b902509j

Cozens AL, Yezzi MJ, Kunzelmann K, Ohrui T, Chin L, Eng K, Finkbeiner WE, Widdicombe JH, Gruenert DC: CFTR expression and chloride secretion in polarized immortal human bronchial epithelial cells. Am J Respir Cell Mol Biol 1994, 10: 38–47.

Boisvieux-Ulrich E, Sourdeval M, Marano F: CD437, a synthetic retinoid, induces apoptosis in human respiratory epithelial cells via caspase-independent mitochondrial and caspase-8-dependent pathways both up-regulated by JNK signaling pathway. Exp Cell Res 2005, 307: 76–90. 10.1016/j.yexcr.2005.02.005

Merendino AM, Bucchieri F, Gagliardo R, Daryadel A, Pompeo F, Chiappara G, Santagata R, Bellia V, David S, Farina F, Davies DE, Simon HU, Vignola AM: CD40 ligation protects bronchial epithelium against oxidant-induced caspase-independent cell death. Am J Respir Cell Mol Biol 2006, 35: 155–164. 10.1165/rcmb.2005-0433OC

Sourdeval M, Lemaire C, Deniaud A, Taysse L, Daulon S, Breton P, Brenner C, Boisvieux-Ulrich E, Marano F: Inhibition of caspase-dependent mitochondrial permeability transition protects airway epithelial cells against mustard-induced apoptosis. Apoptosis 2006, 11: 1545–1559. 10.1007/s10495-006-8764-1

Sourdeval M, Lemaire C, Brenner C, Boisvieux-Ulrich E, Marano F: Mechanisms of doxycycline-induced cytotoxicity on human bronchial epithelial cells. Front Biosci 2006, 11: 3036–3048. 10.2741/2031

Morris RE, Ciraolo GM, Cohen DA, Bubel HC: In situ fixation of cultured mouse peritoneal exudate cells: comparison of fixation methods. In Vitro 1980, 16: 136–146. 10.1007/BF02831504

Lemaire C, Andreau K, Souvannavong V, Adam A: Inhibition of caspase activity induces a switch from apoptosis to necrosis. FEBS Lett 1998, 425: 266–270. 10.1016/S0014-5793(98)00252-X

Rothe G, Valet G: Flow cytometric analysis of respiratory burst activity in phagocytes with hydroethidine and 2',7'-dichlorofluorescin. J Leukoc Biol 1990, 47: 440–448.

Naguib YM: Antioxidant activities of astaxanthin and related carotenoids. J Agric Food Chem 2000, 48: 1150–1154. 10.1021/jf991106k

Rundquist I, Olsson M, Brunk U: Cytofluorometric quantitation of acridine orange uptake by cultured cells. Acta Pathol Microbiol Immunol Scand A 1984, 92: 303–309.