Experimental considerations on the cytotoxicity of nanoparticles

Nanomedicine

Volumn 6, Issue 5, 2011, Pages 929-941

  Kong, Bokyung ^a   Seog, Ji Hyun ^a   Graham, Lauren M ^b   Lee, Sang Bok ^a,b  

^a Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

^b University of Maryland   (United States)

Author keywords

agglomeration; cell type; cytotoxicity assay; dose; nanoparticle; toxicity

Indexed keywords

NANOPARTICLE;

ACCURACY; CYTOTOXICITY TEST; DRUG DELIVERY SYSTEM; FALSE NEGATIVE RESULT; FALSE POSITIVE RESULT; HUMAN; NONHUMAN; PARTICLE SIZE; PRIORITY JOURNAL; REVIEW;

ANIMALS; CYTOLOGICAL TECHNIQUES; CYTOTOXINS; HUMANS; NANOPARTICLES; TOXICITY TESTS;

EID: 79960948501     PISSN: 17435889     EISSN: 17486963     Source Type: Journal    
DOI: 10.2217/nnm.11.77     Document Type: Review

References (96)

1. Zrazhevskiy P, Sena M, Gao X. Designing multifunctional quantum dots for bioimaging, detection, and drug delivery. Chem. Soc. Rev. 39, 4326-4354 (2010).
2. Lee JH, Huh YM, Jun Y et al. Artificially engineered magnetic nanoparticles for ultra-sensitive molecular imaging. Nature Med. 13, 95-99 (2006).
3. Thomas CR, Ferris DP, Lee JH et al. Noninvasive remote-controlled release of drug molecules in vitro using magnetic actuation of mechanized nanoparticles. J. Am. Chem. Soc. 132, 10623-10625 (2010).
4. Neuberger T, Schopf B, Hofmann H, Hofmann M, von Rechenberg B. Superparamagnetic nanoparticles for biomedical applications: possibilities and limitations of a new drug delivery system. J. Magn. Magn. Mater. 293, 483-496 (2005). (Pubitemid 40608969)
5. Qian XM, Peng XH, Ansari DO et al. In vivo tumor targeting and spectroscopic detection with surface-enhanced Raman nanoparticle tags. Nat. Biotech. 26, 83-90 (2008).
6. Bai X, Son SJ, Zhang SX et al. Synthesis of superparamagnetic nanotubes as MRI contrast agents and for cell labeling. Nanomedicine 3, 163-174 (2008). (Pubitemid 351621747)
7. Son SJ, Bai X, Nan A, Ghandehari H, Lee SB. Template synthesis of multifunctional nanotubes for controlled release. J. Control. Release 114, 143-152 (2006). (Pubitemid 44291850)
8. Son SJ, Reichel J, He B, Schuchman M, Lee SB. Magnetic nanotubes for magnetic-field-assisted bioseparation, biointeraction, and drug delivery. J. Am. Chem. Soc. 127, 7316-7317 (2005). (Pubitemid 40746010)
9. Mitchell DT, Lee SB, Trofin L et al. Smart nanotubes for bioseparations and biocatalysis. J. Am. Chem. Soc. 124, 11864-11865 (2002).
10. He B, Kim SK, Son SJ, Lee SB. Shape-coded silica nanotubes for multiplexed bioassay: rapid and reliable magnetic decoding protocols. Nanomedicine 5, 77-88 (2010).
11. Son SJ, Bai X, Lee SB. Inorganic hollow nanoparticles and nanotubes in nanomedicine Part 1. Drug/gene delivery applications. Drug Discov. Today 12, 650-656 (2007). (Pubitemid 47238640)
12. Webster TJ. Nanomedicine: real commercial potential or just hype? Int. J. Nanomed. 1, 373-374 (2006).
13. Lewinski N, Colvin V, Drezek R. Cytotoxicity of nanoparticles. Small 4, 26-49 (2008).
14. Nel A, Xia T, Mädler L, Li N. Toxic potential of materials at nanolevel. Science 311, 622-627 (2006).
15. Oberdöster G, Oberdöster E, Oberdöster J. Nanotoxicology: an emerging discipline evolving from studies of ultrafine particles. Environ. Health Perspect. 113, 823-839 (2005). (Pubitemid 40984181)
16. Subcommittee on Nanoscale Science, Engineering, and Technology, Committee on Technology, National Science and Technology Council: National Nanotechnology Initiative: Strategy for Nanotechnology-Related Environmental, Health, and Safety Research. 1-102 (2008).
17. Chithrani BD, Ghazani AA, Chan WCW. Determining the size and shape dependence of gold nanoparticle uptake into mammalian cells. Nano. Lett. 6, 662-668 (2006).
18. Murphy CJ, Gole AM, Stone JW et al. Gold nanoparticles in biology: beyond toxicity to cellular imaging. Acc. Chem. Res. 41, 1721-1730 (2008).
19. Hussain SM, Hess KL, Gearhart JM, Geiss KT, Schlager JJ. In vitro toxicity of nanoparticles in BRL 3A rat liver cells. Toxicol. In vitro 19, 975-983 (2005). (Pubitemid 41563236)
20. Oberdörster G, Stone V, Donaldson K. Toxicology of nanoparticles: a historical perspective. Nanotoxicology 1, 2-25 (2007). (Pubitemid 46570244)
21. Nan A, Bai X, Son SJ, Lee SB, Ghandehari H. Cellular uptake and cytotoxicity of silica nanotubes. Nano. Lett. 8, 2150-2154 (2008).
22. Royal Society and Royal Academy of Engineering: Nanoscience and Nanotechnologies: Opportunities and Uncertainties. 1-127 (2005).
23. Stone V, Johnston H, Schins RPF. Development of in vitro systems for nanotoxicology: methodological considerations. Crit. Rev. Toxicol. 39, 613-626 (2009).
24. Dhawan A, Sharma V. Toxicity assessment of nanomaterials: methods and challenges. Anal. Bioanal. Chem. 398, 589-605 (2010).
25. Teeguarden JG, Hinderliter PM, Orr G, Thrall BD, Pounds JG. Particokinetics in vitro: dosimetry considerations for in vitro nanoparticle toxicity assessments. Toxicol. Sci. 95, 300-312 (2007). (Pubitemid 46152602)
26. Wörle-Knirsch JM, Pulskamp K, Krug HF. Oops they did it again! Carbon nanotubes hoax scientists in viability assays. Nano. Lett. 6, 1261-1268 (2006). (Pubitemid 44013492)
27. Casey A, Herzog E, Davoren M, Lyng FM, Byrne HJ, Chambers G. Spectroscopic analysis confirms the interactions between single walled carbon nanotubes and various dyes commonly used to assess cytotoxicity. Carbon 45, 1425-1432 (2007). (Pubitemid 46829030)
28. Ciofani G, Danti S, D'Alessandro D, Moscato S, Menciassi A. Assessing cytotoxicity of boron nitride nanotubes: interference with the MTT assay. Biochem. Biophys. Res. Comm. 394, 405-411 (2010).
29. Park MVDZ, Annema W, Salvati A et al. In vitro developmental toxicity test detects inhibition of stem cell differentiation by silica nanoparticles. Toxicol. Appl. Pharm. 240, 108-116 (2009).
30. Tolnai Gy, Csempesz F, Kabai-Faix M et al. Preparation and characterization of surface-modified silica-nanoparticles. Langmuir 17, 2683-2687 (2001). (Pubitemid 35330520)
31. Huang LM, Wang ZB, Sun JY et al. Fabrication of ordered porous structures by self-assembly of zeolite nanocrystals. J. Am. Chem. Soc. 122, 3530-3531 (2000).
32. Brown CC, Kamal M, Nasreen N et al. Influence of shape, adhesion and simulated lung mechanics on amorphous silica nanoparticle toxicity. Adv. Powder Technol. 18, 69-79 (2007). (Pubitemid 46473727)
33. Fortner JD, Lyon DY, Sayes CM et al. C60 in water: nanocrystal formation and microbial response. Environ. Sci. Technol. 39, 4307-4316 (2005). (Pubitemid 40770264)
34. Gulson B, Wong H. Stable isotopic tracing - a way forward for nanotechnology. Environ. Health Perspect. 114, 1486-1488 (2006). (Pubitemid 44509643)
35. Limbach LK, Li Y, Grass RN et al. Oxide nanoparticle uptake in human lung fibroblasts: effects of particle size, agglomeration, and diffusion at low concentrations. Environ. Sci. Technol. 39, 9370-9376 (2005). (Pubitemid 41741229)
36. Lisunova MO, Lebovka NI, Melezhyk OV, Boiko YP. Stability of the aqueous suspensions of nanotubes in the presence of nonionic surfactant. J. Colloid Interface Sci. 299, 740-746 (2006). (Pubitemid 44208990)
37. Díaz B, Sánchez-Espinel C, Arruebo M et al. Assessing methods for blood cell cytotoxic responses to inorganic nanoparticles and nanoparticle aggregates. Small 4, 2025-2034 (2008).
38. Chang JS, Chang KLB, Hwang DF, Kong ZL. In vitro cytotoxicity of silica nanoparticles at high concentrations strongly depends on the metabolic activity type of the cell line. Environ. Sci. Technol. 41, 2064-2068 (2007). (Pubitemid 46449243)
39. Moriguchia T, Yanoa K, Hokarib S, Sonodac M. Fullerene effect of repeated application of C60 combined with UVA radiation onto hairless mouse back skin. Fullerene Sci. Technol. 7, 195-209 (1999).
40. Tsuchiya T, Oguri I, Yamakoshi Y, Miyata N. Novel harmful effects of [60]fullerene on mouse embryos in vitro and in vivo. FEBS Lett. 393, 139-145 (1996). (Pubitemid 26298248)
41. Ueng TH, Kang JJ, Wang HW, Cheng YW. Suppression of microsomal cytochrome P450-dependent monooxygenases and mitochondrial oxidative phosphorylation by fullerenol, a polyhydroxylated fullerene C60. Toxicol. Lett. 93, 29-37 (1997).
42. Maynard AD, Kuempel ED. Airborne nanostructured particles and occupational health. J. Nanopart. Res. 7, 587-614 (2005). (Pubitemid 41767360)
43. Adamson IYR, Prieditis H, Vincent R. Pulmonary toxicity of an atmospheric particulate sample is due to the soluble fraction. Toxicol. Appl. Pharmacol. 157, 43-50 (1999). (Pubitemid 29250252)
44. Valavanidis A, Fiotakis K, Vlachogianni T. Airborne particulate matter and human health: toxicological assessment and importance of size and composition of particles for oxidative damage and carcinogenic mechanisms. J. Environ. Sci. Health 26, 339-362 (2008). (Pubitemid 352790465)
45. Liao CM, Chiang YH, Chio CP. Assessing the airborne titanium dioxide nanoparticle-related exposure hazard at workplace. J. Hazard Mater. 162, 57-95 (2009).
46. Powers M. Nanomedicine and nano device pipeline surges 68%. Nanoiotech. News 2006(1), 1-69 (2006)
47. Nemmar A, Hoylaerts MF, Hoet PH et al. Ultrafine particles affect experimental thrombosis in an in vivo hamster model. Am. J. Respir. Crit. Care Med. 166, 998-1004 (2002). (Pubitemid 35193233)
48. Oberdörster G, Sharp Z, Atudorei V et al. Extrapulmonary translocation of ultrafine carbon particles following whole-body inhalation exposure of rats. J. Toxicol. Environ. Health A 65, 1531-1543 (2002). (Pubitemid 35217499)
49. Vickers AE, Rose K, Fisher R, Saulnier M, Sahota P, Bentley P. Kidney slices of human and rat to characterize cisplatin-induced injury on cellular pathways and morphology. Toxicol. Pathol. 32, 577-590 (2004). (Pubitemid 39258463)
50. Chou CC, Riviere JE, Monteiro-Riviere NA. The cytotoxicity of jet fuel aromatic hydrocarbons and dose-related interleukin-8 release from human epidermal keratinocytes. Arch. Toxicol. 77, 384-391 (2003). (Pubitemid 36960473)
51. Oberdörster G, Maynard A, Donaldson K et al. Principles for characterizing the potential human health effects from exposure to nanomaterials: elements of a screening strategy. Part. Fibre Toxicol. 2, 1-35 (2005).
52. Donaldson K, Stone V, Tran CL, Kreyling W, Borm PJA. A new frontier in particle toxicology relevant to both the workplace and general environment and to consumer safety. Occup. Environ. Med. 61, 727-728 (2004).
53. Donaldson K, Tran CL. Inflammation caused by particles and fibres. Inhal. Toxicol. 14, 5-27 (2002).
54. Nel A, Xia T, Mädler L, Li N. Toxic potential of nanomaterials at nanolevel. Science 311, 622-674 (2006).
55. Dobrovolskaia MA, McNeil SE. Immunological properties of engineered nanomaterials. Nature Nanotech. 2, 469-478 (2007). (Pubitemid 47220069)
56. Rothen-Rutishauser BM, Kiama SG, Gehr P. 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 (2005). (Pubitemid 40478303)
57. Jepson MA, Clark MA. Studying M cells and their role in infection. Trends Microbiol. 6, 359-365 (1998). (Pubitemid 28473196)
58. Chithrani BD, Chan WCW. Elucidating the mechanism of cellular uptake and removal of protein-coated gold nanoparticles of different sizes and shapes. Nano Lett. 7, 1542-1450 (2007).
59. Pan Y, Neuss S, Leifert A, Fischler M, Wen F, Simon U. Size-dependent cytotoxicity of gold nanoparticles. Small 3, 1941-1949 (2007). (Pubitemid 350099867)
60. Powers KW, Palazuelos M, Moudgil BM, Roberts SM. Characterization of the size, shape, and state of dispersion of nanoparticles for toxicological studies. Nanotoxicology 1, 42-51 (2007). (Pubitemid 46570246)
61. Wang SG, Lu WT, Tovmachenko O, Rai US, Yu HT, Ray PC. Challenge in understanding size and shape dependent toxicity of gold nanomaterials in human skin keratinocytes. Chem. Phys. Lett. 463, 145-149 (2008).
62. Wang S, Lu W, Tovmachenko O, Rai US, Yu H, Ray PC. Challenge in understanding size and shape dependent toxicity of gold nanomaterials in human skin keratinocytes. Chem. Phys. Lett. 463, 145-149 (2008).
63. Keller AA, Wang H, Zhou D et al. Stability and aggregation of metal oxide nanoparticles in natural aqueous matrices. Environ. Sci. Technol. 44, 1962-1967 (2010).
64. Auffan M, Bottero JY, Chaneac C, Rose J. Inorganic manufactured nanoparticles: how their physicochemical properties influence their biological effects in aqueous environments. Nanomedicine (Lond.) 5, 999-1007 (2010).
65. Bagwe RP, Hilliard LR, Tan WH. Surface modification of silica nanoparticles to reduce aggregation and nonspecific binding. Langmuir 22, 4357-4362 (2006).
66. Zhang Y, Kohler N, Zhang MQ. Surface modification of superparamagnetic magnetite nanoparticles and their intracellular uptake. Biomaterials 23, 1553-1561 (2002). (Pubitemid 34158578)
67. Gref R, Luck M, Quellec P et al. 'Stealth' corona-core nanoparticles surface modified by polyethylene glycol (PEG): influences of the corona (PEG chain length and surface density) and of the core composition on phagocytic uptake and plasma protein adsorption. Colloid. Surf. B 18, 301-313 (2000). (Pubitemid 30479870)
68. Kohler N, Fryxell GE, Zhang MQ. A bifunctional poly(ethylene glycol) silane immobilized on metallic oxide-based nanoparticles for conjugation with cell targeting agents. J. Am. Chem. Soc. 126, 7206-7211 (2004). (Pubitemid 38747770)
69. Horie M, Nishio K, Kato H, Shinohara N, Nakamura A, Fujita K. In vitro evaluation of cellular responses induced by stable fullerene C-60 medium dispersion. J. Biochem. 148, 289-298 (2010).
70. Skebo JE, Grabinski CM, Schrand AM, Schlager JJ, Hussain SM. Assessment of metal nanoparticle agglomeration, uptake, and interaction using high-illuminating system. Int. J. Toxicol. 26, 135-141 (2007). (Pubitemid 46514925)
71. Ding P, Pacek AW. De-agglomeration of silica nanoparticles in the presence of surfactants. J. Disp. Sci. Technol. 29, 593-599 (2008). (Pubitemid 351494126)
72. Tang E, Tian B, Zheng E, Fu C, Cheng G. Preparation of zinc oxide nanoparticle via uniform precipitation method and its surface modification by methacryloxypropyltrimethoxysilane. Chem. Eng. Comm. 195, 479-491 (2008).
73. Ma DL, Hugener TA, Siegel RW et al. Influence of nanoparticle surface modification on the electrical behavior of polyethylene nanocomposites. Nanotechnology 16, 724-731 (2005). (Pubitemid 40666573)
74. Tantra R, Tompkins J, Quincey P. Characterisation of the de-agglomeration effects of bovine serum albumin on nanoparticles in aqueous suspension. Collid. Surf. A 75, 275-281 (2010).
75. Jonston HJ, Semmler-Behnke M, Brown DM, Kreyling W, Tran L, Stone V. Evaluating the uptake and intracellular fate of polystyrene nanoparticles by primary and hepatocyte cell lines in vitro. Toxicol. Appl. Pharmacol. 242, 66-78 (2010).
76. Thomassen LCJ, Aerts A, Rabolli V, Lison D, Gonzalez L, Kirsch-Volders M. Synthesis and characterization of stable monodisperse silica nanoparticle sols for in vitro cytotoxicity testing. Langmuir 26, 329-335 (2010).
77. Braeckmans K, Buyens K, Bouquet W, Vervaet C, Joye P, De Vos F. Sizing nanomatter in biological fluids by fluorescence single particle tracking. Nano Lett. 10, 4435-4442 (2010).
78. Alkilany AM, Nagaria PK, Hexel CR, Shaw TJ, Murphy CJ, Wyatt MD. Cellular uptake and cytotoxicity of gold nanorods: molecular origin of cytotoxicity and surface effects. Small 5, 701-708 (2009).
79. Shvedova AA, Kisin ER, Mercer R, Murray AR, Johnson VJ, Potapovich AI. Unusual inflammatory and fibrogenic pulmonary responses to single-walled carbon nanotubes in mice. Am. J. Physiol. Lung Cell Mol. Physiol. 289, L698-L708 (2005). (Pubitemid 41504399)
80. Pulskamp K, Diabatè S, Krug HF. Carbon nanotubes show no sign of acute toxicity but induce intracellular reactive oxygen species in dependence on contaminants. Toxicol. Lett. 168, 58-74 (2007). (Pubitemid 44909723)
81. Müller K, Skepper JN, Posfai M et al. Effect of ultrasmall superparamagnetic iron oxide nanoparticles (Ferumoxtran-10) on human monocyte-macrophages in vitro. Biomaterials 28, 1629-1642 (2007). (Pubitemid 46098969)
82. Shukla R, Bansal V, Chaudhary M, Basu A, Bhonde RR, Sastry M. Biocompatibility of gold nanoparticles and their endocytotic fate inside the cellular compartment: a microscopic overview. Langmuir 21, 10644-10654 (2005). (Pubitemid 41692144)
83. Moss OR, Wong VA. When nanoparticles get in the way: impact of projected area on in vivo and in vitro macrophage function. Inhal. Toxicol. 18, 711-716 (2006).
84. Gulson B, Wong H. Stable isotopic tracing - a way forward for nanotechnology. Environ. Health Perspect. 114, 1486-1488 (2006). (Pubitemid 44509643)
85. Morrow P. International Commission on Radiological Protection (ICRP) task group on lung dynamics, depostion and retention models for internal dosimetry of the human respiratory tract. Health Phys. 12, 173-207 (1996).
86. Asgharian B, Anjilvel S. A multiple-path model of fiber deposition in the rat lung. Toxicol. Sci. 44, 80-86 (1998). (Pubitemid 28378052)
87. Casey A, Herzog E, Davoren M, Lyng FM, Byrne HJ, Chambers G. Spectroscopic analysis confirms the interactions between single walled carbon nanotubes and various dyes commonly used to assess cytotoxicity. Carbon 45, 1425-1532 (2007).
88. Shukla S, Priscilla A, Banerjee M, Bhonde RR, Ghatak J, Satyam PV. Porous gold nanospheres by controlled transmetalation reaction: a novel material for application in cell imaging. Chem. Mater. 17, 5000-5005 (2005). (Pubitemid 41476044)
89. Monteiro-Riviere NA, Inman AO, Oldenburg SJ. Interactions of aluminum nanoparticles with human epidermal keratinocytes. J. Appl. Toxicol. 30, 276-285 (2010).
90. Samberg ME, Siekkinen AR, Oldenburg SJ, Monteiro-Riviere NA. Evaluation of silver nanoparticle toxicity in skin in vivo and keratinocytes in vitro. Environ. Health Perspect. 118, 407-413 (2010).
91. Davis RR, Lockwood PE, Hobbs DT, Messer RL, Price RJ, Lewis JB. In vitro biological effects of sodium titanate materials. J. Biomed. Mater. Res. B 83, 505-511 (2007). (Pubitemid 350005023)
92. Aam BB, Fonnum F. Carbon black particles increase reactive oxyge species formation in rat alveolar macrophages in vitro. Arch. Toxicol. 81, 441-446 (2007). (Pubitemid 46980502)
93. Park MVDZ, Annema W, Salvati A, Lesniak A, Elsaesser A, Barnes C. In vitro developmental toxicity test detects inhibition of stem cell differentiation by silica nanoparticles. Toxicol. Appl. Pharmacol. 240, 108-116 (2009).
94. Jones CF, Grainger DW. In vitro assessments of nanomaterial toxicity. Adv. Drug Deliv. Rev. 61(6), 438-456 (2009).
95. Park MV, Lankveld DP, Van Loveren H, De Jong WH. The status of in vitro toxicity studies in the risk assessment of nanomaterials. Nanomedicine (Lond.) 4(6), 669-685 (2009).
96. Dhawan A, Sharma V. Toxicity assessment of nanomaterials: methods and challenges. Anal. Bioanal. Chem. 398(2), 589-605 (2010).