Cellular and molecular responses of E. fetida cœlomocytes exposed to TiO2 nanoparticles
Source abstract
Abstract
An in vitro approach using cœlomocytes of Eisenia fetida was investigated to evaluate toxicity of TiO2 nanoparticles. Cœlomocytes were exposed to well-dispersed suspension of small aggregates (130 nm) of TiO2 nanoparticles (1–25 μg/ml) during 4, 12 and 24 h. Intracellular localisation suggested that the main route of uptake was endocytosis. Cellular responses showed that TiO2 nanoparticles were not cytotoxic and had no effect on phagocytosis at any of the four concentrations for each time tested. Concerning molecular responses, an increase of fetidin and metallothionein mRNA expression was observed starting from 4 h of exposure. In contrast, expression of coelomic cytolytic factor mRNA decreased for 10 and 25 μg/ml after 4 h. Superoxide dismutase, catalase and glutathione-S-transferase expression were not modified suggesting that oxidative stress was not induced by TiO2 in our experimental conditions. This in vitro approach showed that TiO2 nanoparticles were taken up by cœlomocytes and they could modify the molecular response of immune and detoxification system.
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Research context
OpenAlex topics: Nanoparticles: synthesis and applications · Advanced Nanomaterials in Catalysis
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References (73)
Show source-provided references
1. Adams LK, Lyon DY, Alvarez PJJ (2006) Comparative eco-toxicity of nanoscale TiO2, SiO2, and ZnO water suspensions. Water Res 40(19):3527–3532. doi: 10.1016/j.watres.2006.08.00410.1016/j.watres.2006.08.004 ↗
2. Aitken RJ, Chaudhry MQ, Boxall ABA, Hull M (2006) Manufacture and use of nanomaterials: current status in the UK and global trends. Occup Med 56:300–30610.1093/occmed/kql051 ↗
3. Allouni ZE, Cimpan MR, Høl PJ, Skodvin T, Gjerdet NR (2009) Agglomeration and sedimentation of TiO2 nanoparticles in cell culture medium. Colloids Surf B 68(1):83–87. doi: 10.1016/j.colsurfb.2008.09.01410.1016/j.colsurfb.2008.09.014 ↗
4. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:389–3402. doi: 10.1093/nar/25.17.338910.1093/nar/25.17.3389 ↗
5. Asensio V, Kille P, Morgan AJ, Soto M, Marigomez I (2007) Metallothionein expression and neutral red uptake as biomarkers of metal exposure and effect in Eisenia fetida and Lumbricus terrestris exposed to Cd. Eur J Soil Biol 43(S1):S233–S238. doi: 10.1016/j.ejsobi.2007.08.02210.1016/j.ejsobi.2007.08.022 ↗
6. Bae T-H, Tak T-M (2005) Effect of TiO2 nanoparticles on fouling mitigation of ultrafiltration membranes for activated sludge filtration. J Membr Sci 249:1–8. doi: 10.1016/j.memsci.2004.09.008.ISSN:0376-738810.1016/j.memsci.2004.09.008 ↗
7. Barillet S, Simon-Deckers A, Herlin-Boime N, Mayne-L’Hermite M, Reynaud C, Cassio D, Gouget B, Carriere M (2010) Toxicological consequences of TiO2, SiC nanoparticles and multi-walled carbon nanotubes exposure in several mammalian cell types: an in vitro study. J Nanopart Res 12(1):61–73. doi: 10.1007/s11051-009-9694-y10.1007/s11051-009-9694-y ↗
8. Beschin A, Bilej M, Hanssens F, Raymakersi J, Van Dyck E, Revets H, Brys L, Gomez J, De Baetselier P, Timmermans M (1998) Identification and cloning of a glucan- and lipopolysaccharide binding protein from Eisenia foetida earthworm involved in the activation of prophenoloxidase cascade. J Biol Chem 273(38):24948–24954. doi: 10.1074/jbc.273.38.2494810.1074/jbc.273.38.24948 ↗
9. Beschin A, De Baetselier P, Bilej M (2002) CCF, an invertebrate analogue of TNF, is not related to the other lytic components from Eisenia foetida earthworm. BioEssays 24(10):974–974. doi: 10.1002/bies.1014810.1002/bies.10148 ↗
10. Bigorgne E, Foucaud L, Lapied E, Labille J, Botta C, Sirguey C, Falla J, Rose J, Joner EJ, Rodius F, Nahmani J (2011) Ecotoxicological assessment of TiO2 byproducts on the earthworm Eisenia fetida. Environ Pollut 159(10):2698–2705. doi: 10.1016/j.envpol.2011.05.02410.1016/j.envpol.2011.05.024 ↗
11. Bilej M, Rossmann P, Sinkora M, Hanuová R, Beschin A, Raes G, De Baetselier P (1998) Cellular expression of the cytolytic factor in earthworms Eisenia foetida. Immunol Lett 60(1):23–29. doi: 10.1016/S0165-2478(97)00127-210.1016/S0165-2478(97)00127-2 ↗
12. Bilej M, De Baetselier P, Beschin A (2000) Antimicrobial defense of the earthworm. Folia Microbiol 45(10):283–300. doi: 10.1007/BF0281754910.1007/BF02817549 ↗
13. Braydich-Stolle LK, Schaeublin NM, Murdock RC, Jiang J, Biswas P, Schlager JJ, Hussain SM (2008) Crystal structure mediates mode of cell death in TiO2 nanotoxicity. J Nanopart Res 11(6):1361–1374. doi: 10.1007/s11051-008-9523-810.1007/s11051-008-9523-8 ↗
14. Brousseau P, Payette Y, Tryphonas H, Blakley B, Boermans H, Flipo D, Fournier M (1999) Manual of immunological methods. CRC, Boca Raton, FL
15. Brulle F, Mitta G, Cocquerelle C, Vieau D, Lemière S, Leprêtre A, Vandenbulcke F (2006) Cloning and real-time PCR testing of 14 potential biomarkers in Eisenia fetida following cadmium exposure. Environ Sci Technol 40(8):2844–2850. doi: 10.1021/es052299x10.1021/es052299x ↗
16. Brulle F, Mitta G, Leroux R, Lemière S, Leprêtre A, Vandenbulcke F (2007) The strong induction of metallothionein gene following cadmium exposure transiently affects the expression of many genes in Eisenia fetida: a trade-off mechanism? Comp Biochem Physiol C Toxicol Pharmacol 144(4):334–341. doi: 10.1016/j.cbpc.2006.10.00710.1016/j.cbpc.2006.10.007 ↗
17. Brulle F, Cocquerelle C, Wamalah AN, Morgan AJ, Kille P, Leprêtre A, Vandenbulcke F (2008) cDNA cloning and expression analysis of Eisenia fetida (Annelida: Oligochaeta) phytochelatin synthase under cadmium exposure. Ecotoxicol Environ Saf 71(1):47–55. doi: 10.1016/j.ecoenv.2007.10.03210.1016/j.ecoenv.2007.10.032 ↗
18. Canesi L, Ciacci C, Vallotto D, Gallo G, Marcomini A, Pojana G (2010) In vitro effects of suspensions of selected nanoparticles (C60 fullerene, TiO2, SiO2) on Mytilus hemocytes. Aquat Toxicol 96(2):151–158. doi: 10.1016/j.aquatox.2009.10.01710.1016/j.aquatox.2009.10.017 ↗
19. Carmichael J, DeGraff WG, Gazdar AF, Minna JD, Mitchell JB (1987) Evaluation of a tetrazolium-based semiautomated colorimetrie assay: assessment of chemosensitivity testing. Cancer Res 47:936–942
20. Cerenius L, Söderhäll K (2004) The prophenoloxidase-activating system in invertebrates. Immunol Rev 198(1):116–126. doi: 10.1111/j.0105-2896.2004.00116.x10.1111/j.0105-2896.2004.00116.x ↗
21. Cooper EL (2002) The earthworm: a new model with biomedical applications. In: Cooper EL, Beschin A, Bilej M (eds) A new model for analysing antimicrobial peptides with biomedical applications. IOS Press, Amsterdam, pp 3–26
22. Cooper EL, Roch P (2003) Earthworm immunity: a model of immune competence: The 7th international symposium on earthworm ecology, Cardiff Wales 2002. Pedobiologia 47(5–6):676–688. doi: 10.1078/0031-4056-0024510.1078/0031-4056-00245 ↗
23. Cooper EL, Stein EA (1981) Oligochaete. In: Ratcliffe NA, Rowley AF (eds) Invertebrate blood cells. Acadamic Press, London, pp 75–140
24. Cui Y, Gong X, Duan Y, Li N, Hu R, Liu H, Hong M, Zhou M, Wang L, Wang H, Hong F (2010) Hepatocyte apoptosis and its molecular mechanisms in mice caused by titanium dioxide nanoparticles. J Hazard Mater 183(1–3):874–880. doi: 10.1016/j.jhazmat.2010.07.10910.1016/j.jhazmat.2010.07.109 ↗
25. Dallinger R (1996) Metallothionein research in terrestrial invertebrates: synopsis and perspectives. Comp Biochem Physiol C 113(2):125–133. doi: 10.1016/0742-8413(95)02078-0
26. Eyambe GE, Goven AJ, Fitzpatrick LC, Venables BJ, Cooper EL (1991) A non-invasive technique for sequential collection of earthworm (Lumbricus terrestris) leukocytes during subchronic immunotoxicity studies. Lab Anim 25(1):61–67. doi: 10.1258/00236779178080809510.1258/002367791780808095 ↗
27. Federici G, Shaw BJ, Handy RD (2007) Toxicity of titanium dioxide nanoparticles to rainbow trout (Oncorhynchus mykiss): gill injury, oxidative stress, and other physiological effects. Aquat Toxicol 84(4):415–430. doi: 10.1016/j.aquatox.2007.07.00910.1016/j.aquatox.2007.07.009 ↗
28. Fotakis G, Timbrell JA (2006) In vitro cytotoxicity assays: comparison of LDH, neutral red, MTT and protein assay in hepatoma cell lines following exposure to cadmium chloride. Toxicol Lett 160(2):171–177. doi: 10.1016/j.toxlet.2005.07.00110.1016/j.toxlet.2005.07.001 ↗
29. Foucaud L, Wilson MR, Brown DM, Stone V (2007) Measurement of reactive species production by nanoparticles prepared in biologically relevant media. Toxicol Lett 174(1–3):1–9. doi: 10.1016/j.toxlet.2007.08.00110.1016/j.toxlet.2007.08.001 ↗
30. Fournier M, Cyr D, Blakley B, Boermans H, Brousseau P (2000) Phagocytosis as a biomarker of immunotoxicity in wildlife species exposed to environmental xenobiotics. Am Zoo 40:412–420. doi: 10.1093/icb/40.3.41210.1668/0003-1569(2000)040[0412:PAABOI]2.0.CO;2 ↗
31. French RA, Jacobson AR, Kim B, Isley SL, Penn LR, Baveye PC (2009) Influence of ionic strength, pH, and cation valence on aggregation kinetics of titanium dioxide nanoparticles. Env Sci Technol 43(5):1354–1359. doi: 10.1021/es802628n10.1021/es802628n ↗
32. Goven AJ, Venables BJ, Fitzpatrick LC (2005) Earthworms as ecosentinels for chemical-induced immunotoxicity. In: Tryphonas H, Fournier M, Blakley BR, Smits JEG, Brousseau P (eds) Investigative immunotoxicology. Taylor & Francis, Boca Raton, FL, pp 106–119
33. Gurr J-R, Wang ASS, Chen C-H, Jan K-Y (2005) Ultrafine titanium dioxide particles in the absence of photoactivation can induce oxidative damage to human bronchial epithelial cells. Toxicology 213(1–2):66–73. doi: 10.1016/j.tox.2005.05.00710.1016/j.tox.2005.05.007 ↗
34. Hu CW, Li M, Cui YB, Li DS, Chen J, Yang LY (2010) Toxicological effects of TiO2 and ZnO nanoparticles in soil on earthworm Eisenia fetida. Soil Biol Biochem 42(4):586–591. doi: 10.1016/j.soilbio.2009.12.00710.1016/j.soilbio.2009.12.007 ↗
35. Hussain S, Boland S, Baeza-Squiban A, Hamel R, Thomassen LCJ, Martens JA, Billon-Galland MA, Fleury-Feith J, Moisan F, Pairon J-C, Marano F (2009) Oxidative stress and proinflammatory effects of carbon black and titanium dioxide nanoparticles: role of particle surface area and internalized amount. Toxicology 260(1–3):142–149. doi: 10.1016/j.tox.2009.04.00110.1016/j.tox.2009.04.001 ↗
36. Jang HD, Kim S-K, Kim S-J (2001) Effect of particle size and phase composition of titanium dioxide nanoparticles on the photocatalytic properties. J Nanopart Res 3(2–3):141–147. doi: 10.1023/A:101794833036310.1023/A:1017948330363 ↗
37. Jemec A, Drobne D, Remskar M, Sepcic K, Tisler T (2008) Effects of ingested nano-sized titanium dioxide on terrestrial isopods (Porcellio scaber). Environ Toxicol Chem 27(9):1904–1914. doi: 10.1897/08-036.110.1897/08-036.1 ↗
38. Jiang J, Oberdörster G, Biswas P (2009) Characterization of size, surface charge, and agglomeration state of nanoparticle dispersions for toxicological studies. J Nanopart Res 11:77–89. doi: 10.1007/s11051-008-9446-410.1007/s11051-008-9446-4 ↗
39. Jin C-Y, Zhu B-S, Wang X-F, Lu Q-H (2008) Cytotoxicity of titanium dioxide nanoparticles in mouse fibroblast cells. Chem Res Toxicol 21:1871–1877. doi: 10.1021/tx800179f10.1021/tx800179f ↗
40. Klaine SJ, Alvarez PJJ, Batley GE, Fernandes TF, Handy RD, Lyon DY, Mahendra S, McLaughlin MJ, Lead JR (2008) Nanomaterials in the environment: behavior, fate, bioavailability, and effects. Environ Toxicol Chem 27(9):1825–1851. doi: 10.1897/08-090.110.1897/08-090.1 ↗
41. Köhlerová P, Beschin A, Silerová M, De Baetselier P, Bilej M (2004) Effect of experimental microbial challenge on the expression of defense molecules in Eisenia foetida earthworm. Dev Comp Immunol 28(7–8):701–711. doi: 10.1016/j.dci.2004.01.00110.1016/j.dci.2004.01.001 ↗
42. Lapied E, Moudilou E, Exbrayat J-M, Oughton DH, Joner EJ (2010) Silver nanoparticle exposure causes apoptotic response in the earthworm Lumbricus terrestris (Oligochaeta). Nanomedicine 5(6):975–984. doi: 10.2217/nnm.10.5810.2217/nnm.10.58 ↗
43. Lassegues M, Milochau A, Doignon F, DuPasquier L, Valembois P (1997) Sequence and expression of an Eisenia-fetida-derived cDNA clone that encodes the 40-kDa fetidin antibacterial protein. Eur J Biochem 246(3):756–762. doi: 10.1111/j.1432-1033.1997.00756.x10.1111/j.1432-1033.1997.00756.x ↗
44. Liu X, Sun Z, Chong W, Sun Z, He C (2009) Growth and stress responses of the earthworm Eisenia fetida to Escherichia coli O157:H7 in an artificial soil. Microb Pathog 46(5):266–272. doi: 10.1016/j.micpath.2009.02.00110.1016/j.micpath.2009.02.001 ↗
45. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-[Delta][Delta]CT method. Methods 25(4):402–408. doi: 10.1006/meth.2001.126210.1006/meth.2001.1262 ↗
46. Maleri RA, Fourie F, Reinecke AJ, Reinecke SA (2008) Photometric application of the MTT- and NRR-assays as biomarkers for the evaluation of cytotoxicity ex vivo in Eisenia andrei. Soil Biol Biochem 40(5):1040–1048. doi: 10.1016/j.soilbio.2007.11.02410.1016/j.soilbio.2007.11.024 ↗
47. Mandzy N, Grulke E, Druffel T (2005) Breakage of TiO2 agglomerates in electrostatically stabilized aqueous dispersions. Powder Technol 160(2):121–126. doi: 10.1016/j.powtec.2005.08.02010.1016/j.powtec.2005.08.020 ↗
48. Massicotte R, Robidoux PY, Sauvé S, Flipo D, Mathiot A, Fournier M, Trottier B (2004) Immunotoxicological response of the earthworm Lumbricus terrestris following exposure to cement kiln dusts. Ecotoxicol Environ Saf 59(1):10–16. doi: 10.1016/j.ecoenv.2004.05.00310.1016/j.ecoenv.2004.05.003 ↗
49. Milochau A, Lassègues M, Valembois P (1997) Purification, characterization and activities of two hemolytic and antibacterial proteins from coelomic fluid of the annelid Eisenia fetida andrei. Biochim Biophys Acta 1337(1):123–132. doi: 10.1016/S0167-4838(96)00160-410.1016/S0167-4838(96)00160-4 ↗
50. Monteiller C, Tran L, MacNee W, Faux S, Jones A, Miller B, Donaldson K (2007) The pro-inflammatory effects of low-toxicity low-solubility particles, nanoparticles and fine particles, on epithelial cells in vitro: the role of surface area. Occup Environ Med 64(9):609–615. doi: 10.1136/oem.2005.02480210.1136/oem.2005.024802 ↗
51. Monteiro-Riviere NA, Inman AO, Zhang LW (2009) Limitations and relative utility of screening assays to assess engineered nanoparticle toxicity in a human cell line. Toxicol Appl Pharmacol 234(2):222–235. doi: 10.1016/j.taap.2008.09.03010.1016/j.taap.2008.09.030 ↗
52. Murdock RC, Braydich-Stolle L, Schrand AM, Schlager JJ, Hussain SM (2008) Characterization of nanomaterial dispersion in solution prior to in vitro exposure using dynamic light scattering technique. Toxicol Sci 101(2):239–253. doi: 10.1093/toxsci/kfm24010.1093/toxsci/kfm240 ↗
53. Oberdörster G, Stone V, Donaldson K (2007) Toxicology of nanoparticles: a historical perspective. Nanotoxicology 1:2–25. doi: 10.1080/1743539070131476110.1080/17435390701314761 ↗
54. Pagnout C, Jomini S, Dadhwal M, Caillet C, Thomas F, Bauda P (2012) Role of electrostatic interactions in the toxicity of titanium dioxide nanoparticles toward bacteria. Colloids Surf B Biointerfaces 92:315–321. doi: 10.1016/j.colsurfb.2011.12.01210.1016/j.colsurfb.2011.12.012 ↗
55. Park S, Lee YK, Jung M, Kim KH, Chung N, Ahn E-K, Lim Y, Lee K-H (2007) Cellular toxicity of various inhalable metal nanoparticles on human alveolar epithelial cells. Inhalation Toxicol 19(S1):59–65. doi: 10.1080/0895837070149328210.1080/08958370701493282 ↗
56. Park E-J, Yi J, Chung K-H, Ryu D-Y, Choi J, Park K (2008) Oxidative stress and apoptosis induced by titanium dioxide nanoparticles in cultured BEAS-2B cells. Toxicol Lett 180(3):222–229. doi: 10.1016/j.toxlet.2008.06.86910.1016/j.toxlet.2008.06.869 ↗
57. Procházková P, Silerová M, Felsberg J, Josková R, Beschin A, De Baetselier P, Bilej M (2006) Relationship between hemolytic molecules in Eisenia fetida earthworms. Dev Comp Immunol 30(4):381–392. doi: 10.1016/j.dci.2005.06.01410.1016/j.dci.2005.06.014 ↗
58. R Developement Core Team (2006) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, http://www.R-project.org
59. Rahman Q, Lohani M, Dopp E, Pemsel H, Jonas L, Weiss D, Schiffmann D (2002) Evidence that ultrafine titanium dioxide induces micronuclei and apoptosis in Syrian hamster embryo fibroblasts. Environ Health Perspect 110(8):797–800. doi: org/10.1289/ehp.0211079710.1289/ehp.02110797 ↗
60. Reeves JF, Davies SJ, Dodd NJF, Jha AN (2008) Hydroxyl radicals (OH) are associated with titanium dioxide (TiO2) nanoparticle-induced cytotoxicity and oxidative DNA damage in fish cells. Mutat Res 640(1–2):113–122. doi: 10.1016/j.mrfmmm.2007.12.01010.1016/j.mrfmmm.2007.12.010 ↗
61. Rejman J, Oberle V, Zuhorn IS, Hoekstra D (2004) Size-dependent internalization of particles via the pathways of clathrin- and caveolae-mediated endocytosis. Biochem J 377(1):159–169. doi: 10.1042/BJ2003125310.1042/bj20031253 ↗
62. Renwick LC, Donaldson K, Clouter A (2001) Impairment of alveolar macrophage phagocytosis by ultrafine particles. Toxicol Appl Pharmacol 172(2):119–127. doi: 10.1006/taap.2001.912810.1006/taap.2001.9128 ↗
63. Roh J-Y, Park Y-K, Park K, Choi J (2010) Ecotoxicological investigation of CeO2 and TiO2 nanoparticles on the soil nematode Caenorhabditis elegans using gene expression, growth, fertility, and survival as endpoints. Environ Toxicol Pharmacol 29(2):167–172. doi: 10.1016/j.etap.2009.12.00310.1016/j.etap.2009.12.003 ↗
64. Sauvé S, Fournier M (2005) Age-specific immunocompetence of the earthworm Eisenia andrei: exposure to methylmercury chloride. Ecotoxicol Environ Saf 60(1):67–72. doi: 10.1016/j.ecoenv.2003.12.02210.1016/j.ecoenv.2003.12.022 ↗
65. Sauvé S, Hendawi M, Brousseau P, Fournier M (2002) Phagocytic response of terrestrial and aquatic invertebrates following in vitro exposure to trace elements. Ecotoxicol Environl Saf 52(1):21–29. doi: 10.1006/eesa.2001.212510.1006/eesa.2001.2125 ↗
66. Sayes CM, Wahi R, Kurian PA, Liu Y, West JL, Ausman KD, Warheit DB, Colvin VL (2006) Correlating nanoscale titania structure with toxicity: a cytotoxicity and inflammatory response study with human dermal fibroblasts and human lung epithelial cells. Toxicol Sci 92(1):174–185. doi: 10.1093/toxsci/kfj19710.1093/toxsci/kfj197 ↗
67. Simon-Deckers A, Gouget B, Mayne-L’Hermite M, Herlin-Boime N, Reynaud C, Carrière M (2008) In vitro investigation of oxide nanoparticle and carbon nanotube toxicity and intracellular accumulation in A549 human pneumocytes. Toxicology 253(1–3):137–146. doi: 10.1016/j.tox.2008.09.00710.1016/j.tox.2008.09.007 ↗
68. Singh S, Shi T, Duffin R, Albrecht C, van Berlo D, Höhr D, Fubini B, Martra G, Fenoglio I, Borm PJA, Schins RPF (2007) Endocytosis, oxidative stress and IL-8 expression in human lung epithelial cells upon treatment with fine and ultrafine TiO2: role of the specific surface area and of surface methylation of the particles. Toxicol Appl Pharmacol 222(2):141–151. doi: 10.1016/j.taap.2007.05.00110.1016/j.taap.2007.05.001 ↗
69. Stone V, Johnston H, Schins RPF (2009) Development of in vitro systems for nanotoxicology: methodological considerations. Crit Rev Toxicol 39(7):613–626. doi: 10.1080/1040844090312097510.1080/10408440903120975 ↗
70. Thurn KT, Arora H, Paunesku T, Wu A, Brown EMB, Doty C, Kremer J, Woloschak G (2011) Endocytosis of titanium dioxide nanoparticles in prostate cancer PC-3M cells. Nanomedicine 7(2):123–130. doi: 10.1016/j.nano.2010.09.00410.1016/j.nano.2010.09.004 ↗
71. Ville P, Roch P, Cooper EL, Narbonne J-F (1997) Immuno-modulator effects of PCBs, carbaryl and 2,4 D in the earthworm Eisenia fetida andrei. Arch Environ Contam Toxicol 32(2):291–297. doi: 10.1016/S0145-305X(97)88569-210.1007/s002449900187 ↗
72. Wagner AJ, Bleckmann CA, Murdock RC, Schrand AM, Schlager JJ, Hussain SM (2007) Cellular interaction of different forms of aluminum nanoparticles in rat alveolar macrophages. J Phys Chem B 111(25):7353–7359. doi: 10.1021/jp068938n10.1021/jp068938n ↗
73. Wang JJ, Sanderson BJS, Wang H (2007) Cyto- and genotoxicity of ultrafine TiO2 particles in cultured human lymphoblastoid cells. Mutat Res 628(2):99–106. doi: 10.1016/j.mrgentox.2006.12.00310.1016/j.mrgentox.2006.12.003 ↗