Development of in vitro systems for nanotoxicology: Methodological considerations in vitro methods for nanotoxicology Vicki Stone et al.

Critical Reviews in Toxicology

Volumn 39, Issue 7, 2009, Pages 613-626

  Stone, Vicki ^a   Johnston, Helinor ^a   Schins, Roel P F ^b  

^a EDINBURGH NAPIER UNIVERSITY   (United Kingdom)

^b HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

Cytotoxicity; Genotoxicity; In vitro; Inflammation; Nanoparticles; Protocols

Indexed keywords

NANOPARTICLE; REACTIVE OXYGEN METABOLITE;

BIOLOGICAL ACTIVITY; CYTOTOXICITY; GENOTOXICITY; IN VITRO STUDY; NANOTOXICOLOGY; OXIDATIVE STRESS; PRACTICE GUIDELINE; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; HUMANS; NANOSTRUCTURES; NANOTECHNOLOGY; TOXICITY TESTS;

EID: 70350503605     PISSN: 10408444     EISSN: 15476898     Source Type: Journal    
DOI: 10.1080/10408440903120975     Document Type: Review

References (79)

1. Albrecht C, Knaapen AM, Becker A, Hohr D, Haberzettl P, van Schooten FJ, Borm PJ, Schins RP (2005). Te crucial role of particle surface reactivity in respirable quartz-induced reactive oxygen/nitrogen species formation and APE/Ref-1 induction in rat lung. Respir Res 6:129.
2. Bartosz G (2006). Use of spectroscopic probes for detection of reactive oxygen species. Clin Chim Acta 368:53-76.
3. Borm PJ, Schins RP, Albrecht C (2004). Inhaled particles and lung cancer, part B: paradigms and risk assessment. Int J Cancer 110:3-14.
4. British Standards Institution (2007). Terminology for nanomaterials. PAS 136.
5. BSI, London. Brown DM, Donaldson K, Borm PJ, Schins RP, Denhart M, Gilmour P, Jimenez LA, Stone V (2004). Calcium and reactive oxygen species-mediated activation of transcription factors and TNFa cytokine gene expression in macrophages exposed to ultrafne particles. Am J Physiol Lung Cell Mol Physiol 286:L344-L353.
6. Brown DM, Hutchison L, Donaldson K, MacKenzie SJ, Dick CA, Stone V (2007a). Te efect of oxidative stress on macrophages and lung epithelial cells: the role of phosphodiesterases 1 and 4. Toxicol Lett 168:1-6.
7. Brown DM, Kinloch IA, Bangert U, Windle AH, Walter DM, Walker GS, Scotchford CA, Donaldson K, Stone V (2007b). An in vitro study of the potential of carbon nanotubes and nanofbres to induce infammation mediators and frustrated phagocytosis. Carbon 45:1743-1756.
8. Clift MJ, Rothen-Rutishauser B, Brown DM, Dufn R, Donaldson K, Proudfoot L, Guy K, Stone V (2008). Te impact of diferent nanoparticle surface chemistry and size on uptake and toxicity in a murine macrophage cell line. Toxicol Appl Pharmacol 232:418-427.
9. Da Costa AO, de Assis MC, Marques EA, Plotkowski MC (1999). Comparative analysis of three methods to assess viability of mammalian cells in culture. Biocell 23:65-72.
10. Davis JM, Addison J, Bolton RE, Donaldson K, Jones AD, Smith T (1986). Te pathogenicity of long versus short fbre samples of amosite asbestos administered to rats by inhalation and intraperitoneal injection. Br J Exp Pathol 67:415-430.
11. Dick CA, Brown DM, Donaldson K, Stone V (2003). Te role of free radicals in the toxic and infammatory efects of four diferent ultrafne particle types. Inhal Toxicol 15:39-52.
12. Dikalov S, Griendling LK, Harrison DG (2007). Measurement of reactive oxygen species in cardiovascular studies. Hypertension 49:717-727.
13. Donaldson K, Tran CL, Jimenez LA, Dufn R, Newby D, Mills N, MacNee W, Stone V (2005). Combustion-derived nanoparticles: a critical review of their toxicology following inhalation exposure. Part Fibre Toxicol 2:1-14.
14. Donaldson K, Borm PJ, Oberdorster G, Pinkerton KE, Stone V Tran CL (2008). Concordance between in vitro and in vivo dosimetry in the proinfammatory efects of low-toxicity, low-solubility particles: the key role of the proximal alveolar region. Inhal Toxicol 20:53-62.
15. Driscoll KE, Deyo LC, Carter JM, Howard BW, Hassenbein DG, Bertram TA (1997). Efects of particle exposure and particle-elicited infammatory cells on mutation in rat alveolar epithelial cells. Carcinogenesis 18:423-430.
16. Dufn R, Tran CL, Clouter A, Brown DM, MacNee W, Stone V, Donaldson K (2002). Te importance of surface area and specifc reactivity in the acute pulmonary infammatory response to particles. Ann Occup Hyg 46(Suppl 1):242-245.
17. Dufn R, Tran L, Brown D, Stone V Donaldson K (2007). Proinfammo genic efects of low-toxicity and metal nanoparticles in vivo and in vitro: highlighting the role of particle surface area and surface reactivity. Inhal Toxicol 19:849-856.
18. Faulkner K, Fridovich I (1993). Luminol and lucigenin as detectors for O2.-. Free Radic Biol Med 15:447-451.
19. Fenech M (1997). Te advantages and disadvantages of the cytokinesis-block micronucleus method. Mutat Res 392:11-18.
20. Fenoglio I, Greco G, Tomatis M, Muller J, Raymundo-Pinero E, Beguin F, Fonseca A, Nagy JB, Lison D, Fubini B (2008). Structural defects play a major role in the acute lung toxicity of multiwall carbon nanotubes: physicochemical aspects. Chem Res Toxicol 21:1690-1697.
21. Ferin J, Oberdoster G, Penney DP, Soderholm SC, Gelein R, Piper HC (1990). Increased pulmonary toxicity of ultrafne particles? I. Particle clearance, translocation, morphology. J Aerosol Sci 21:381-384.
22. Foucaud L, Wilson MR, Brown DM, Stone V (2007). Measurement of reactive species production by nanoparticles prepared in biologically relevant media. Toxicol Lett 174:1-9.
23. Gehr P, Blank F, Rothen-Rutishauser BM (2006). Fate of inhaled particles after interaction with the lung surface. Paediatr Respir Rev 7 (Suppl 1):S73-S75.
24. Geiser M, Kapp N, Schurch S, Kreyling W, Schulz H, Semmler M, Im Hof V, Heyder J, Gehr P (2005). Ultrafne particles cross celullar membranes by non-phagocytic mechanisms in lungs and in cultured cells. Environ Health Perspect 113:1555-1560.
25. Gilmour PS, Brown DM, Beswick PH, MacNee W, Rahman I, Donaldson K (1997). Free radical activity of industrial fbers: role of iron in oxidative stress and activation of transcription factors. Environ Health Perspect 105(Suppl 5):1313-1317.
26. Greim H, Borm P, Schins R, Donaldson K, Driscoll K, Hartwig A, Kuempel E, Oberdorster G, Speit G (2001). Toxicity of fbers and particles. Report of the workshop held in Munich, Germany, 26-27 October 2000. Inhal Toxicol 13:737-754.
27. Gurr JR, Want AS, Chen CH, Jan KY (2005). Ultrafne titanium dioxide particles in the absence of photoactivation can induce oxidative damage to human bronchial epithelial cells. Toxicology 213:66-73.
28. Haberzettl P, Schins RP, Hohr D, Wilhelmi V, Borm PJ, Albrecht C (2008). Impact of the FcgammaII-receptor on quartz uptake and infammatory response by alveolar macrophages. Am J Physiol Lung Cell Mol Physiol 294:L1137-L1148.
29. Hill IM, Beswick PH, Donaldson K (1995). Diferential release of superoxide anions by macrophages treated with long and short fbre amosite asbestos is a consequence of diferential afnity for opsonin. Occup Environ Med 52:92-96.
30. Hohr D, Steinfartz Y, Schins RP, Knaapen AM, Martra G, Fubini B, Borm PJ (2002). Te surface area rather than the surface coating determines the acute infammatory response after instillation of fne and ultrafne TiO2 in the rat. Int J Hyg Environ Health 205:239-244.
31. Jacobsen NR, Pojana G, White P, Moller P, Cohn CA, Korsholm KS, Vogel U, Marcomini A, Loft S, Wallin H (2008). Genotoxicity, cytotoxicity, and reactive oxygen species induced by single-walled carbon nanotubes and C(60) fullerenes in the FE1-Mutatrade mark Mouse lung epithelial cells. Environ Mol Mutagen 49:476-487.
32. Jepson MA, Clark MA (1998). Studying M cells and their role in infection. Trends Microbiol 6:359-365.
33. Jones C, Grainger DW (2009). In vitro assessments of nanomaterial toxicity. Adv Drug Deliv Rev 61:438-456.
34. Karlsson HL, Cronholm P, Gustafsson J, Möller L (2008). Copper oxide nanoparticles are highly toxic: a comparison between metal oxide nanoparticles and carbon nanotubes. Chem Res Toxicol 21:1726-1732.
35. Kirsch-Volders M, Sofuni T, Aardema M, Albertini S, Eastmond D, Fenech M, Ishidate M Jr, Kirchner S, Lorge E, Morita T, Norppa H, Surralles J, Vanhauwaert A, Wakata A (2003). Report from the in vitro micronucleus assay working group. Mutat Res 540:153-163.
36. Kisin ER, Murray AR, Keane MJ, Shi XC, Schwegler-Berry D, Gorelik O, Arepalli S, Castranova V, Wallace WE, Kagan VE, Shvedova A (2007). Single-walled carbon nanotubes: geno-and cytotoxic efecs in lung fbroblast V79 cells. J Toxicol Environ Health 70:2071-2079.
37. Landsiedel R, Kapp MD, Schulz M, Wiench K, Oesch F (2009). Genotoxicity investigations on nanomaterials: methods, preparation and characterization of test material, potential artifacts and limitations- many questions, some answers. Mutat Res 681:241-258.
38. Li H, van Berlo D, Shi T, Speit G, Knaapen AM, Borm PJ, Albrecht C, Schins RP (2008). Curcumin protects against cytotoxic and infammatory efects of quartz particles but causes oxidative DNA damage in a rat lung epithelial cell line. Toxicol Appl Pharmacol 227:115-124.
39. Li XY, Brown D, Smith S, MacNee W, Donaldson K (1999). Short-term infammatory responses following intratracheal instillation of fne and ultrafne carbon black in rats. Inhal Toxicol 11:709-731.
40. Marnett LJ (2000). Oxyradicals and DNA damage. Carcinogenesis 21:316-370.
41. Maynard AD, Aitken RJ, Butz T, Colvin V, Donaldson K, Oberdorster G, Philbert MA, Ryan J, Seaton A, Stone V, Tinkle SS, Tran L, Walker NJ, Warheit DB (2006). Safe handling of nanotechnology. Nature 444:267-269.
42. McGregor DB, Baan RA, Partensky C, Rice JM, Wilbourn JD (2000). Evaluation of the carcinogenic risks to humans associated with surgical implants and other foreign bodies-a report of an IARC Monographs Programme Meeting. International Agency for Research on Cancer. Eur J Cancer 36:307-313.
43. Mills NL, Tornqvist H, Gonzalez MC, Vink E, Robinson SD, Soderberg S, Boon NA, Donaldson K, Sandstrom T, Blomberg A, Newby DE (2007). Ischemic and thrombotic efects of dilute diesel-exhaust inhalation in men with coronary heart disease. N Engl J Med 357:1075-1082.
44. Monteiro-Riviere NA, Tran CL (2007). Nanotoxicology. Characterization, Dosing and Health Efects. Informa Healthcare, London.
45. 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 234:222-235.
46. Mori T, Takada H, Ito S, Matsubayashi K, Miwa N, Sawaguchi T (2006). Preclinical studies on safety of fullerene upon acute oral administration and evaluation for no mutagenesis. Toxicology 225:48-54.
47. Mossman T. (1983). Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65:55-63.
48. Mroz RM, Schins RP, Li H, Jimenez LA, Drost EM, Holownia A, MacNee W, Donaldson K (2008). Nanoparticle-driven DNA damage mimics irradiation-related carcinogenesis pathways. Eur Respir J 31:241-251.
49. Muller J, Decordier I, Hoet PH, Lombaert N, Tomassen L, Huaux F, Lison D, Kirsch-Volders M (2008). Clastogenic and aneugenic efects of multi-wall carbon nanotubes in epithelial cells. Carcinogenesis 29:427-433.
50. Myhre O, Andersen JM, Aarnes H, Fonnum F (2003). Evaluation of the probes 2',7'-dichlorofuorescin diacetate, luminol, and lucigenin as indicators of reactive species formation. Biochem Pharmacol 65:1575-1582.
51. Netzlaf F, Lehr CM, Wertz PW, Schaefer UF (2005). Te human epidermis models EpiSkin, SkinEthic and EpiDerm: an evaluation of morphology and their suitability for testing phototoxicity, irritancy, corrosivity, and substance transport. Eur J Pharm Biopharm 60:167-178.
52. Oberdoerster G, Ferin J, Finkelstein J, Wade P, Corson N (1990). Increased pulmonary toxicity of ultrafne particles? II. Lung lavage studies. J Aerosol Sci 21:384-387.
53. Oberdoerster G, Stone V, Donaldson K (2007). Toxicology of nanoparticles: a historical perspective. Nanotoxicology 1:2-25.
54. Papageorgiou I, Brown C, Schins R, Singh S, Newson R, Davis S, Fisher J, Ingham E, Case CP (2007). Te efect of nano-and micron-sized particles of cobalt-chromium alloy on human fbroblasts in vitro. Biomaterials 28:2946-2958.
55. Peters A, Wichmann HE, Tuch T, Heinrich J, Heyder J (1997). Respiratory efects are associated with the number of ultrafne particles. Am J Respir Crit Care Med 155:1376-1383.
56. Porter D, Sriram K, Wolfarth M, Jeferson A, Schwegler-Berry D, Andrew ME, Castranova V (2008). A biocompatible medium for nanoparticle dispersion. Nanotoxicology 2:144-154.
57. Powers KW, Palazuelos M, Moudgil BM, Roberts SM (2007). Characterization of the size, shape, and state of dispersion of nanoparticles for toxicological studies. Nanotoxicology 1:42-51.
58. Prahalad AK, Inmon J, Dailey LA, Madden MC, Ghio AJ, Gallagher JE (2001). Air pollution particles mediated oxidative DNA base damage in a cell free system and in human airway epithelial cells in relation to particulate metal content and bioreactivity. Chem Res Toxicol 14:879-887.
59. Rahman Q, Lohani M, Dopp E, Pemsel H, Jonas L, Weiss DG, Schifmann D (2002). Evidence that ultrafne titanium dioxide induces micronuclei and apoptosis in Syrian hamster embryo fbroblasts. Environ Health Perspect 110:797-800.
60. Rothen-Rutishauser BM, Kiama SG, Gehr P (2005). A three-dimensional cellular model of the human respiratory tract to study the interaction with particles. Am J Respir Cell Mol Biol 32:281-289.
61. Sayes CM, Liang F, Hudson JL, Mendez J, Guo W, Beach JM, Moore VC, Doyle CD, West JL, Billups WE, Ausman KD, Colvin VL (2006). Functionalization density dependence of single-walled carbon nanotubes cytotoxicity in vitro. Toxicol Lett 161:135-142.
62. Schins RP, McAlinden A, MacNee W, Jimenez LA, Ross JA, Guy K, Faux SP, Donaldson K (2000). Persistent depletion of I kappa B alpha and interleukin-8 expression in human pulmonary epithelial cells exposed to quartz particles. Toxicol Appl Pharmacol 167:107-117.
63. Schins RP, Dufn R, Hohr D, Knaapen AM, Shin T, Weishaupt C, Stone V, Donaldson K, Borm PJ (2002). Surface modifcation of quartz inhibits toxicity, particle uptake, and oxidative DNA damage in human lung epithelial cells. Chem Res Toxicol 15:1166-1173.
64. Schins RP, Knaapen AM (2007). Genotoxicity of poorly soluble particles. Inhal Toxicol 19(Suppl 1):189-198.
65. Seaton A, MacNee W, Donaldson K, Godden D (1995). Particulate air pollution and acute health efects. Lancet 345:176-178.
66. Singh S, Shi T, Dufn R, Albrecht C, van Berlo D, Hohr D, Fubini B, Martra G, Fenoglio I, Borm PJ, Schins RP (2007). Endocytosis, oxidative stress and IL-8 expression in human lung epithelial cells upon treatment with fne and ultrafne TiO2: role of the specifc surface area and of surface methylation of the particles. Toxicol Appl Pharmacol 222:141-151.
67. Speit G (2002). Appropriate in vitro test conditions for genotoxicity testing of fbers. Inhal Toxicol 14:79-90.
68. Stoeger T, Reinhard C, Takenaka S, Schroeppel A, Karg E, Ritter B, Heyder J, Schulz H (2006). Instillation of six diferent ultrafne carbon particles indicates a surface area threshold dose for acute lung infammation in mice. Environ Health Perspect 114:328-333.
69. Stone V, Shaw J, Brown DM, MacNee W, Faux SP, Donaldson K (1998). Te role of oxidative stress in the prolonged inhibitory efect of ultrafne carbon black on epithelial cell function. Toxicol In Vitro 12:649-659.
70. Stone V, Tuinman M, Vamvakopoulos JE, Shaw J, Brown D, Petterson S, Faux SP, Borm P, MacNee W, Michaelangeli F, Donaldson K (2000). Increased calcium infux in a monocytic cell line on exposure to ultrafne carbon black. Eur Respir J 15:297-303.
71. Sydlik U, Bierhals K, Souf M, Abel J, Schins RP, Unfried K (2006). Ultrafne carbon particles induce apoptosis and proliferation in rat lung epithelial cells via specifc signaling pathways both using EGF-R. Am J Physiol Lung Cell Mol Physiol 291:L725-L733.
72. Tice RR, Agurell E, Anderson D, Burlinson B, Hartmann A, Kobayashi H, Miyamae Y, Rojas E, Ryu JC, Sasaki YF (2000). Single cell gel/comet assay: guidelines for in vitro and in vivo genetic toxicology testing. Environ Mol Mutagen 35:206-221.
73. Unfried K, Albrecht C, Klotz LO, von Mikecz A, Grether-Beck S, Schins RPF (2007). Cellular responses to nanoparticles: target structures and mechanisms. Nanotoxicology 1:52-71.
74. Vainio H, Magee P, McGregor D, McMichael A, eds. (1992). Mechanisms of Carcinogenesis in Risk Identifcation. IARC Scientifc Publications No. 116. IARC, Lyon.
75. Warheit DB, Hoke RA, Finlay C, Donner EM, Reed KL, Sayes CM (2007). Development of a base set of toxicity tests using ultrafne TiO2 particles as a component of nanoparticle risk management. Toxicol Lett 171:99-110.
76. Wilson MR, Lightbody JH, Donaldson K, Sales J, Stone V (2002). Interactions between ultrafne particles and transition metals in vivo and in vitro. Toxicol Appl Pharmacol 184:172-179.
77. Worle-Knirsch JM, Pulskamp K, Krug HF (2006). Oops they did it again! Carbon nanotubes hoax scientists in viability assays. Nano Lett 6:1261-1268.
78. Xiao GG, Wang M, Li N, Loo JA, Nel AE (2003). Use of proteomics to demonstrate a hierarchical oxidative stress response to diesel exhaust particle chemicals in a macrophage cell line. J Biol Chem 278:50781-50790.
79. Yoshinaga K, Obata H, Jurukovski V, Mazzieri R, Chen Y, Zilberberg L, Huso D, Melamed J, Prijatelj P, Todorovic V, Dabovic B, Rifkin DB (2008). Perturbation of transforming growth factor (TGF)-beta1 association with latent TGF-beta binding protein yields infammation and tumors. Proc Natl Acad Sci USA 105:18758-18763.