Rational design of gold nanoparticle toxicology assays: A question of exposure scenario, dose and experimental setup

Nanomedicine

Volumn 9, Issue 13, 2014, Pages 1971-1989

  Taylor, Ulrike ^a   Rehbock, Christoph ^b   Streich, Carmen ^b   Rath, Detlef ^a   Barcikowski, Stephan ^b  

^a FEDERAL RESEARCH INSTITUTE FOR ANIMAL HEALTH   (Germany)

^b UNIVERSITY OF DUISBURG ESSEN   (Germany)

Author keywords

colloids; dosimetry; functional toxicity; implant debris; ligand; nanogold; nanomaterial; particle characterization; surfactant

Indexed keywords

GOLD NANOPARTICLE; REACTIVE OXYGEN METABOLITE; GOLD; LIGAND; METAL NANOPARTICLE;

APOPTOSIS; BIOASSAY; BIOCOMPATIBILITY; BUILDING MATERIAL; CELL COUNT; CELL DIFFERENTIATION; CELL FUNCTION; CELL METABOLISM; CELL VIABILITY; CENTRIFUGATION; CYTOTOXICITY; DENSITY GRADIENT CENTRIFUGATION; EXPOSURE; FERTILIZATION; GENE EXPRESSION; GENOTOXICITY; GOLD STANDARD; GRANULOSA CELL; HUMAN; HYDRODYNAMICS; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; INTERNALIZATION; LIGHT SCATTERING; NANOTOXICOLOGY; NONHUMAN; OOCYTE MATURATION; ORGAN WEIGHT; PARTICLE SIZE; PRONUCLEUS; REPRODUCTIVE TOXICITY; REVIEW; ROENTGEN SPECTROSCOPY; SCANNING ELECTRON MICROSCOPY; SPERM; SPERMATOZOON; STEM CELL; SURFACE PROPERTY; TOXICITY TESTING; TRANSMISSION ELECTRON MICROSCOPY; ULTRACENTRIFUGATION; DOSE RESPONSE;

BIOLOGICAL ASSAY; DOSE-RESPONSE RELATIONSHIP, DRUG; GOLD; HUMANS; LIGANDS; METAL NANOPARTICLES; PARTICLE SIZE; SURFACE PROPERTIES;

EID: 84908296376     PISSN: 17435889     EISSN: 17486963     Source Type: Journal    
DOI: 10.2217/nnm.14.139     Document Type: Review

References (104)

1. Dykman L, Khlebtsov N. Gold nanoparticles in biomedical applications: Recent advances and perspectives. Chem. Soc. Rev. 41(6), 2256-2282 (2012).
2. Boisselier E, Astruc D. Gold nanoparticles in nanomedicine: Preparations, imaging, diagnostics, therapies and toxicity. Chem. Soc. Rev. 38(6), 1759-1782 (2009).
3. Barchanski A, Taylor U, Klein S, Petersen S, Rath D, Barcikowski S. Golden perspective: Application of laser-generated gold nanoparticle conjugates in reproductive biology. Reprod. Domest. Anim. 46, 42-52 (2011).
4. Zhang HY, Ji ZX, Xia T et al. Use of metal oxide nanoparticle band gap to develop a predictive paradigm for oxidative stress and acute pulmonary inflammation. ACS Nano 6(5), 4349-4368 (2012).
5. Connor EE, Mwamuka J, Gole A, Murphy CJ, Wyatt MD. Gold nanoparticles are taken up by human cells but do not cause acute cytotoxicity. Small 1(3), 325-327 (2005).
6. 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(23), 10644-10654 (2005).
7. Tiedemann D, Taylor U, Rehbock C et al. Reprotoxicity of gold, silver, and gold-silver alloy nanoparticles on mammalian gametes. Analyst 139(5), 931-942 (2014).
8. Cho WS, Cho M, Jeong J et al. Acute toxicity and pharmacokinetics of 13 nm-sized PEG-coated gold nanoparticles. Toxicol. Appl. Pharmacol. 236(1), 16-24 (2009).
9. Truong L, Saili KS, Miller JM, Hutchison JE, Tanguay RL. Persistent adult zebrafish behavioral deficits results from acute embryonic exposure to gold nanoparticles. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 155(2), 269-274 (2012).
10. Kim KT, Zaikova T, Hutchison JE, Tanguay RL. Gold nanoparticles disrupt zebrafish eye development and pigmentation. Toxicol. Sci. 133(2), 275-288 (2013).
11. Pan Y, Neuss S, Leifert A et al. Size-dependent cytotoxicity of gold nanoparticles. Small 3(11), 1941-1949 (2007).
12. Oberdorster G, Oberdorster E, Oberdorster J. Nanotoxicology: An emerging discipline evolving from studies of ultrafine particles. Environ. Health Perspect. 113(7), 823-839 (2005).
13. Organisation for Economic Co-operation and Development. Guidance on Sample Preparation and Dosimetry for the Safety Testing of Manufactured Nanomaterials. Series on the Safety of Manufactured Nanomaterials No. 36. OECD Publications Service, Paris, France (2012).
14. Schleh C, Semmler-Behnke M, Lipka J et al. Size and surface charge of gold nanoparticles determine absorption across intestinal barriers and accumulation in secondary target organs after oral administration. Nanotoxicology 6(1), 36-46 (2012).
15. Lipka J, Semmler-Behnke M, Sperling RA et al. Biodistribution of PEG-modified gold nanoparticles following intratracheal instillation and intravenous injection. Biomaterials 31(25), 6574-6581 (2010).
16. Chen CY, Li YF, Qu Y, Chai ZF, Zhao YL. Advanced nuclear analytical and related techniques for the growing challenges in nanotoxicology. Chem. Soc. Rev. 42(21), 8266-8303 (2013).
17. Khlebtsov N, Dykman L. Biodistribution and toxicity of engineered gold nanoparticles: A review of in vitro and in vivo studies. Chem. Soc. Rev. 40(3), 1647-1671 (2011).
18. Stone V, Johnston H, Schins RPF. Development of in vitro systems for nanotoxicology: Methodological considerations. Crit. Rev. Toxicol. 39(7), 613-626 (2009).
19. Horie M, Kato H, Fujita K, Endoh S, Iwahashi H. in vitro evaluation of cellular response induced by manufactured nanoparticles. Chem. Res. Toxicol. 25(3), 605-619 (2012).
20. Joris F, Manshian BB, Peynshaert K, De Smedt SC, Braeckmans K, Soenen SJ. Assessing nanoparticle toxicity in cell-based assays: Influence of cell culture parameters and optimized models for bridging the in vitro-in vivo gap. Chem. Soc. Rev. 42(21), 8339-8359 (2013).
21. Taylor U, Klein S, Petersen S, Kues W, Barcikowski S, Rath D. Nonendosomal cellular uptake of ligand-free, positively charged gold nanoparticles. Cytometry A 77A(5), 439-446 (2010).
22. Alkilany AM, Murphy CJ. Toxicity and cellular uptake of gold nanoparticles: What we have learned so far?. J. Nanopart. Res. 12(7), 2313-2333 (2010).
23. Taylor U, Barchanski A, Petersen S et al. Gold nanoparticles interfere with sperm functionality by membrane adsorption without penetration. Nanotoxicology doi:10.3109/17435390.2013.859321 (2013) (Epub ahead of print).
24. Petersen S, Soller JT, Wagner S et al. Co-Transfection of plasmid DNA and laser-generated gold nanoparticles does not disturb the bioactivity of GFP-HMGB1 fusion protein. J. Nanobiotechnol. 7, 6 (2009).
25. Stelzer R, Hutz RJ. Gold nanoparticles enter rat ovarian granulosa cells and subcellular organelles, and alter in-vitro estrogen accumulation. J. Reprod. Dev. 55(6), 685-690 (2009).
26. Li WQ, Wang F, Liu ZM, Wang YC, Wang J, Sun F. Gold nanoparticles elevate plasma testosterone levels in male mice without affecting fertility. Small 9(9-10), 1708-1714 (2013).
27. Kim SW, Kwak JI, An YJ. Multigenerational study of gold nanoparticles in Caenorhabditis elegans: Transgenerational effect of maternal exposure. Environ. Sci. Technol. 47(10), 5393-5399 (2013).
28. Wang Y, Aker WG, Hwang HM, Yedjou CG, Yu H, Tchounwou PB. A study of the mechanism of in vitro cytotoxicity of metal oxide nanoparticles using catfish primary hepatocytes and human HepG2 cells. Sci. Total Environ. 409(22), 4753-4762 (2011).
29. Hanley C, Layne J, Punnoose A et al. Preferential killing of cancer cells and activated human T cells using ZnO nanoparticles. Nanotechnology 19(29), 295103 (2008).
30. Bregoli L, Chiarini F, Gambarelli A et al. Toxicity of antimony trioxide nanoparticles on human hematopoietic progenitor cells and comparison to cell lines. Toxicology 262(2), 121-129 (2009).
31. Hackenberg S, Scherzed A, Technau A, Froelich K, Hagen R, Kleinsasser N. Functional responses of human adipose tissue-derived mesenchymal stem cells to metal oxide nanoparticles in vitro. J. Biomed. Nanotechnol. 9(1), 86-95 (2013).
32. Campagnolo L, Fenoglio I, Massimiani M, Magrini A, Pietroiusti A. Screening of nanoparticle embryotoxicity using embryonic stem cells. Methods Mol. Biol. 1058, 49-60 (2013).
33. Steiner S, Mueller L, Popovicheva OB et al. Cerium dioxide nanoparticles can interfere with the associated cellular mechanistic response to diesel exhaust exposure. Toxicol. Lett. 214(2), 218-225 (2012).
34. Eisenbrand G, Pool-Zobel B, Baker V et al. Methods of in vitro toxicology. Food Chem. Toxicol. 40(2-3), 193-236 (2002).
35. Borm P, Klaessig FC, Landry TD et al. Research strategies for safety evaluation of nanomaterials, part V: Role of dissolution in biological fate and effects of nanoscale particles. Toxicol. Sci. 90(1), 23-32 (2006).
36. Nel A, Xia T, Madler L, Li N. Toxic potential of materials at the nanolevel. Science 311(5761), 622-627 (2006).
37. Pan Y, Leifert A, Ruau D et al. Gold nanoparticles of diameter 1.4 nm trigger necrosis by oxidative stress and mitochondrial damage. Small 5(18), 2067-2076 (2009).
38. Coradeghini R, Gioria S, Garcia CP et al. Size-dependent toxicity and cell interaction mechanisms of gold nanoparticles on mouse fibroblasts. Toxicol. Lett. 217(3), 205-216 (2013).
39. 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(1-3), 145-149 (2008).
40. Zhang XD, Wu D, Shen X et al. Size-dependent in vivo toxicity of PEG-coated gold nanoparticles. Int. J. Nanomed. 6, 2071-2081 (2011).
41. Chen YS, Hung YC, Liau I, Huang GS. Assessment of the in vivo toxicity of gold nanoparticles. Nanoscale Res. Lett. 4(8), 858-864 (2009).
42. Patra HK, Banerjee S, Chaudhuri U, Lahiri P, Dasgupta AK. Cell selective response to gold nanoparticles. Nanomedicine 3(2), 111-119 (2007).
43. Albanese A, Tang PS, Chan WCW. The effect of nanoparticle size, shape, and surface chemistry on biological systems. Annu. Rev. Biomed. Eng. 14, 1-16 (2012).
44. Chernousova S, Epple M. Silver as antibacterial agent: Ion, nanoparticle, and metal. Angew. Chem. Int. Ed. Engl. 52(6), 1636-1653 (2013).
45. Alkilany AM, Murphy CJ. Toxicity and cellular uptake of gold nanoparticles: What we have learned so far?. J. Nanopart. Res. 12(7), 2313-2333 (2010).
46. Han X, Corson N, Wade-Mercer P et al. Assessing the relevance of in vitro studies in nanotoxicology by examining correlations between in vitro and in vivo data. Toxicology 297(1-3), 1-9 (2012).
47. Oberdorster G. Pulmonary effects of inhaled ultrafine particles. Int. Arch. Occup. Environ. Health 74(1), 1-8 (2001).
48. Stoeger T, Reinhard C, Takenaka S et al. Instillation of six different ultrafine carbon particles indicates a surface area threshold dose for acute lung inflammation in mice. Environ. Health Perspect. 114(3), 328-333 (2006).
49. Tsoli M, Kuhn H, Brandau W, Esche H, Schmid G. Cellular uptake and toxicity of AU(55) clusters. Small 1(8-9), 841-844 (2005).
50. Teeguarden JG, Hinderliter PM, Orr G, Thrall BD, Pounds JG. Particokinetics in vitro: Dosimetry considerations for in vitro nanoparticle toxicity assessments. Toxicol. Sci. 95(2), 300-312 (2007).
51. Oberdorster G, Ferin J, Lehnert BE. Correlation between particle-size, in-vivo particle persistence, and lung injury. Environ. Health Perspect. 102, 173-179 (1994).
52. Faux SP, Tran C-L, Miller BG, Jones AD, Monteiller C, Donaldson K. In vitro Determinants of Particulate Toxicity: The Dose-Metric for Poorly Soluble Dusts. Health and Safety Executive Books, Sudbury, UK (2003).
53. Barcikowski S, Walter J, Hahn A et al. Picosecond and femtosecond laser machining may cause health risks related to nanoparticle emission. J. Laser Micro Nanoeng. 4(3), 159-164 (2009).
54. Hinderliter PM, Minard KR, Orr G et al. ISDD: A computational model of particle sedimentation, diffusion and target cell dosimetry for in vitro toxicity studies. Part. Fibre Toxicol. 7(1), 36 (2010).
55. Siddiqi NJ, Abdelhalim MA, El-Ansary AK, Alhomida AS, Ong WY. Identification of potential biomarkers of gold nanoparticle toxicity in rat brains. J. Neuroinflammation 9, 123 (2012).
56. Rehbock C, Jacobi J, Gamrad L et al. Current state on laser synthesis of metal and alloy nanoparticles, qualified as ligand-free reference materials for nano-Toxicological assays. Beilstein J. Nanotechnol. 5, 1523-1541 (2014).
57. Deloid G, Cohen JM, Darrah T et al. Estimating the effective density of engineered nanomaterials for in vitro dosimetry. Nat. Commun. 5, 3514 (2014).
58. James AE, Driskell JD. Monitoring gold nanoparticle conjugation and analysis of biomolecular binding with nanoparticle tracking analysis (NTA) and dynamic light scattering (DLS). Analyst 138(4), 1212-1218 (2013).
59. Choi SY, Jeong S, Jang SH et al. In vitro toxicity of serum protein-Adsorbed citrate-reduced gold nanoparticles in human lung adenocarcinoma cells. Toxicol. In vitro 26(2), 229-237 (2012).
60. Grade S, Eberhard J, Neumeister A et al. Serum albumin reduces the antibacterial and cytotoxic effects of hydrogel-embedded colloidal silver nanoparticles. RSC Adv. 2(18), 7190-7196 (2012).
61. Hahn A, Fuhlrott J, Loos A, Barcikowski S. Cytotoxicity and ion release of alloy nanoparticles. J. Nanopart. Res. 14(1), 1-10 (2012).
62. Albanese A, Chan WCW. Effect of gold nanoparticle aggregation on cell uptake and toxicity. ACS Nano 5(7), 5478-5489 (2011).
63. Cho EC, Zhang Q, Xia Y. The effect of sedimentation and diffusion on cellular uptake of gold nanoparticles. Nat. Nanotechnol. 6(6), 385-391 (2011).
64. Camden JP, Dieringer JA, Wang YM et al. Probing the structure of single-molecule surface-enhanced Raman scattering hot spots. J. Am. Chem. Soc. 130(38), 12616-12617 (2008).
65. Dominguez-Medina S, Blankenburg J, Olson J, Landes CF, Link S. Adsorption of a protein mono layer via hydrophobic interactions prevents nanoparticle aggregation under harsh environmental conditions. ACS Sustain. Chem. Eng. 1(7), 833-842 (2013).
66. Perreault F, Melegari SP, Fuzinatto CF et al. Toxicity of PAMAM-coated gold nanoparticles in different unicellular models. Environ. Toxicol. 29(3), 328-336 (2014).
67. Vetten MA, Tlotleng N, Rascher DT et al. Label-free in vitro toxicity and uptake assessment of citrate stabilised gold nanoparticles in three cell lines. Part. Fibre Toxicol. 10, 50 (2013).
68. Zhang XD, Wu D, Shen X, Liu PX, Fan FY, Fan SJ. In vivo renal clearance, biodistribution, toxicity of gold nanoclusters. Biomaterials 33(18), 4628-4638 (2012).
69. Dobrovolskaia MA, Patri AK, Zheng J et al. Interaction of colloidal gold nanoparticles with human blood: Effects on particle size and analysis of plasma protein binding profiles. Nanomedicine 5(2), 106-117 (2009).
70. Van Den Broek B, Ashcroft B, Oosterkamp TH, Van Noort J Parallel Nanometric 3D Tracking of Intracellular Gold Nanorods Using Multifocal Two-photon Microscopy. Nano Lett. 13(3), 980-986 (2013).
71. Bao CC, Beziere N, Del Pino P et al. Gold nanoprisms as optoacoustic signal nanoamplifiers for in vivo bioimaging of gastrointestinal cancers. Small 9(1), 68-74 (2013).
72. Abraham GE, Himmel PB. Management of rheumatoid arthritis: Rationale for the use of colloidal metallic gold. J. Nutr. Environ. Med. 7(4), 295-305 (1997).
73. Turkevich J, Garton G, Stevenson PC. The color of colloidal gold. J. Colloid Sci. 9(6), S26-S35 (1954).
74. Frens G. Controlled nucleation for regulation of particle-size in monodisperse gold suspensions. Nat. Phys. Sci. 241(105), 20-22 (1973).
75. Krebs HA. Chemical composition of blood plasma and serum. Annu. Rev. Biochem. 19, 409-430 (1950).
76. Cho WS, Cho MJ, Jeong J et al. Acute toxicity and pharmacokinetics of 13 nm-sized PEG-coated gold nanoparticles. Toxicol. Appl. Pharmacol. 236(1), 16-24 (2009).
77. Goodman CM, Mccusker CD, Yilmaz T, Rotello VM. Toxicity of gold nanoparticles functionalized with cationic and anionic side chains. Bioconjugate Chem. 15(4), 897-900 (2004).
78. Leifert A, Pan Y, Kinkeldey A, et al. Differential hERG ion channel activity of ultrasmall gold nanoparticles. Proc Natl Acad Sci. USA 110(20), 8004-8009 (2013).
79. Park J-W, Shumaker-Parry JS. Structural study of citrate layers on gold nanoparticles: Role of intermolecular interactions in stabilizing nanoparticles. J. Am. Chem. Soc. 136(5), 1907-1921 (2014).
80. Brewer SH, Glomm WR, Johnson MC, Knag MK, Franzen S. Probing BSA binding to citrate-coated gold nanoparticles and surfaces. Langmuir 21(20), 9303-9307 (2005).
81. Ojea-Jimenez I, Puntes V. Instability of cationic gold nanoparticle bioconjugates: The role of citrate ions. J. Am. Chem. Soc. 131(37), 13320-13327 (2009).
82. Misra SK, Dybowska A, Berhanu D, Luoma SN, Valsami-Jones E. The complexity of nanoparticle dissolution and its importance in nanotoxicological studies. Sci. Total Environ. 438, 225-232 (2012).
83. Sweeney SF, Woehrle GH, Hutchison JE. Rapid purification and size separation of gold nanoparticles via diafiltration. J. Am. Chem. Soc. 128(10), 3190-3197 (2006).
84. Dalwadi G, Benson HA, Chen Y. Comparison of diafiltration and tangential flow filtration for purification of nanoparticle suspensions. Pharm. Res. 22(12), 2152-2162 (2005).
85. Balasubramanian SK, Yang LM, Yung LYL, Ong CN, Ong WY, Yu LE. Characterization, purification, and stability of gold nanoparticles. Biomaterials 31(34), 9023-9030 (2010).
86. Amendola V, Meneghetti M. Laser ablation synthesis in solution and size manipulation of noble metal nanoparticles. Phys. Chem. Chem. Phys. 11(20), 3805-3821 (2009).
87. Amendola V, Meneghetti M. What controls the composition and the structure of nanomaterials generated by laser ablation in liquid solution?. Phys. Chem. Chem. Phys. 15(9), 3027-3046 (2013).
88. Barcikowski S, Compagnini G. Advanced nanoparticle generation and excitation by lasers in liquids. Phys. Chem. Chem. Phys. 15(9), 3022-3026 (2013).
89. Barcikowski S, Devesa F, Moldenhauer K. Impact and structure of literature on nanoparticle generation by laser ablation in liquids. J. Nanopart. Res. 11(8), 1883-1893 (2009).
90. Muto H, Yamada K, Miyajima K, Mafune F. Estimation of surface oxide on surfactant-free gold nanoparticles laser-Ablated in water. J. Phys. Chem. C 111(46), 17221-17226 (2007).
91. Merk VM, Rehbock C, Becker F, Hagemann U, Nienhaus H, Barcikowski S. In situ non-DLVO stabilization of surfactant-free, plasmonic gold nanoparticles: The effect of Hofmeister's anions. Langmuir 30(15) 4213-4222 (2014).
92. Wagener P, Schwenke A, Barcikowski S. How citrate ligands affect nanoparticle adsorption to microparticle supports. Langmuir 28(14), 6132-6140 (2012).
93. Cederquist KB, Keating CD. Curvature effects in DNA: Au nanoparticle conjugates. ACS Nano 3(2), 256-260 (2009).
94. Barchanski A, Hashimoto N, Petersen S, Sajti CL, Barcikowski S. Impact of spacer and strand length on oligonucleotide conjugation to the surface of ligand-free laser-generated gold nanoparticles. Bioconjugate Chem. 23(5), 908-915 (2012).
95. Tenzer S, Docter D, Kuharev J et al. Rapid formation of plasma protein corona critically affects nanoparticle pathophysiology. Nat. Nanotechnol. 8(10), 772-781 (2013).
96. Barbour PSM, Stone MH, Fisher J. A hip joint simulator study using simplified loading and motion cycles generating physiological wear paths and rates. Proc. Inst. Mech. Eng. H 213(6), 455-467 (1999).
97. Brown C, Williams S, Tipper JL, Fisher J, Ingham E. Characterisation of wear particles produced by metal on metal and ceramic on metal hip prostheses under standard and microseparation simulation. J. Mater. Sci. Mater. Med. 18(5), 819-827 (2007).
98. Doorn PF, Campbell PA, Worrall J, Benya PD, McKellop HA, Amstutz HC. Metal wear particle characterization from metal on metal total hip replacements: Transmission electron microscopy study of periprosthetic tissues and isolated particles. J. Biomed. Mater. Res. 42(1), 103-111 (1998).
99. Behl B, Papageorgiou I, Brown C et al. Biological effects of cobalt-chromium nanoparticles and ions on dural fibroblasts and dural epithelial cells. Biomaterials 34(14), 3547-3558 (2013).
100. Menendez-Manjon A, Barcikowski S. Hydrodynamic size distribution of gold nanoparticles controlled by repetition rate during pulsed laser ablation in water. Appl. Surf. Sci. 257(9), 4285-4290 (2011).
101. Hahn A, Barcikowski S. Production of bioactive nanomaterial using laser generated nanoparticles. J. Laser Micro Nanoeng. 4(1), 51-54 (2009).
102. Jakobi J, Petersen S, Menendez-Manjon A, Wagener P, Barcikowski S. Magnetic alloy nanoparticles from laser ablation in cyclopentanone and their embedding into a photoresist. Langmuir 26(10), 6892-6897 (2010).
103. Zhang J, Oko DN, Garbarino S et al. Preparation of PtAu alloy colloids by laser ablation in solution and their characterization. J. Phys. Chem. C 116(24), 13413-13420 (2012).
104. Jakobi J, Menendez-Manjon A, Chakravadhanula VSK, Kienle L, Wagener P, Barcikowski S. Stoichiometry of alloy nanoparticles from laser ablation of PtIr in acetone and their electrophoretic deposition on PtIr electrodes. Nanotechnology 22(14), 145601 (2011).